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Philip Henry Howe

TitleChair, Department of Biochemistry
InstitutionMedical University of South Carolina
DepartmentBiochemistry and Molecular Biology
AddressP.O. Box MSC 509
501A
173 Ashley Ave.
Phone843-792-4687
Fax843-792-8304
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    Collapse Overview 
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    Research in the Howe laboratory is focused on understanding the signaling pathways activated by transforming growth factor ß1 (TGFß1), interleukin-like EMT inducer (ILEI) and Wnt in cellular models of differentiation and cancer. One major area of interest is a recently identified signaling pathway whereby TGFß regulates epithelial-mesenchymal transitions (EMT) and metastasis through a post-transcriptional mechanism involving the regulation of an RNA binding protein, heterogeneous ribonucleoprotein E1 (hnRNP E1). We are focused on how TGFß regulation of hnRNP E1 phosphorylation not only regulates translational silencing of select mRNAs involved in EMT/metastasis but also of lncRNAs that may also contribute to tumor progression. Candidate mRNA targets and lncRNAs are actively being pursued and one mRNA target in particular, the cytokine ILEI, has become a major focus of the laboratory. Aside from its known role in EMT, relatively little is known regarding ILEI. We have identified ILEI as a potent stem factor in breast epithelium and are actively investigating the molecular mechanisms through which it mediates its progenitor effects.

    In another focus area we are investigating the role of the adaptor molecule, disabled-2 (Dab2), as a mediator of the cross-talk between the TGFß and Wnt signaling pathways. We have shown that the tumor suppressor functions of Dab2 are mediated thru its attenuation of canonical Wnt/ß-catenin signaling by selectively recruiting the Wnt co-receptor LRP6 to the clathrin-dependent endocytic route, thereby sequestering it from caveolin-mediated endocytosis and signaling. TGFß levels in cells and tissues regulates Dab2 expression and thereby regulates, thru Dab2, Wnt signaling. We are currently investigating this cross-talk in the developing zebrafish and in animal tumor models. We have also made the recent observation that Dab2 regulates TGFß-induced apoptosis and autophagy. We have shown that mechanistically Dab2 serves as a molecular switch to control whether cells undergo apoptosis or autophagy in response to TGFß, and significantly this switch may be underlie chemosensitivity and acquired-resistance during tumorigenesis.

    Collapse keywords
    Cytokine signaling in cancer, Cancer stem cells

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    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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    1. Woosley AN, Dalton AC, Hussey GS, Howley BV, Mohanty BK, Grelet S, Dincman T, Bloos S, Olsen SK, Howe PH. TGFß promotes breast cancer stem cell self-renewal through an ILEI/LIFR signaling axis. Oncogene. 2019 May; 38(20):3794-3811. PMID: 30692635.
      View in: PubMed
    2. Howley BV, Howe PH. Metastasis-associated upregulation of ER-Golgi trafficking kinetics: regulation of cancer progression via the Golgi apparatus. Oncoscience. 2018 May; 5(5-6):142-143. PMID: 30035168.
      View in: PubMed
    3. Noguchi K, Dincman TA, Dalton AC, Howley BV, McCall BJ, Mohanty BK, Howe PH. Interleukin-like EMT inducer (ILEI) promotes melanoma invasiveness and is transcriptionally up-regulated by upstream stimulatory factor-1 (USF-1). J Biol Chem. 2018 07 20; 293(29):11401-11414. PMID: 29871931.
      View in: PubMed
    4. Janakiraman H, House RP, Gangaraju VK, Diehl JA, Howe PH, Palanisamy V. The Long (lncRNA) and Short (miRNA) of It: TGFß-Mediated Control of RNA-Binding Proteins and Noncoding RNAs. Mol Cancer Res. 2018 04; 16(4):567-579. PMID: 29555893.
      View in: PubMed
    5. Howley BV, Howe PH. TGF-beta signaling in cancer: post-transcriptional regulation of EMT via hnRNP E1. Cytokine. 2019 Jun; 118:19-26. PMID: 29396052.
      View in: PubMed
    6. Emetu S, Troiano M, Goldmintz J, Tomberlin J, Grelet S, Howe PH, Korey C, Geslain R. Metabolic Labeling and Profiling of Transfer RNAs Using Macroarrays. J Vis Exp. 2018 01 16; (131). PMID: 29364226.
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    7. Grelet S, Geslain R, Howe PH. EMT does not work regular shifts. Cell Cycle. 2018; 17(2):141-142. PMID: 29334820.
      View in: PubMed
    8. Howley BV, Link LA, Grelet S, El-Sabban M, Howe PH. A CREB3-regulated ER-Golgi trafficking signature promotes metastatic progression in breast cancer. Oncogene. 2018 03; 37(10):1308-1325. PMID: 29249802.
      View in: PubMed
    9. Grelet S, Link LA, Howley B, Obellianne C, Palanisamy V, Gangaraju VK, Diehl JA, Howe PH. Addendum: A regulated PNUTS mRNA to lncRNA splice switch mediates EMT and tumour progression. Nat Cell Biol. 2017 11 29; 19(12):1443. PMID: 29184176.
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    10. Qie S, Majumder M, Mackiewicz K, Howley BV, Peterson YK, Howe PH, Palanisamy V, Diehl JA. Fbxo4-mediated degradation of Fxr1 suppresses tumorigenesis in head and neck squamous cell carcinoma. Nat Commun. 2017 11 16; 8(1):1534. PMID: 29142209.
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    11. Gencer S, Oleinik N, Kim J, Panneer Selvam S, De Palma R, Dany M, Nganga R, Thomas RJ, Senkal CE, Howe PH, Ogretmen B. TGF-ß receptor I/II trafficking and signaling at primary cilia are inhibited by ceramide to attenuate cell migration and tumor metastasis. Sci Signal. 2017 Oct 24; 10(502). PMID: 29066540.
      View in: PubMed
    12. Grelet S, Link LA, Howley B, Obellianne C, Palanisamy V, Gangaraju VK, Diehl JA, Howe PH. A regulated PNUTS mRNA to lncRNA splice switch mediates EMT and tumour progression. Nat Cell Biol. 2017 Sep; 19(9):1105-1115. PMID: 28825698.
      View in: PubMed
    13. Grelet S, McShane A, Geslain R, Howe PH. Pleiotropic Roles of Non-Coding RNAs in TGF-ß-Mediated Epithelial-Mesenchymal Transition and Their Functions in Tumor Progression. Cancers (Basel). 2017 Jul 01; 9(7). PMID: 28671581.
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    14. Noguchi K, Dalton AC, Howley BV, McCall BJ, Yoshida A, Diehl JA, Howe PH. Interleukin-like EMT inducer regulates partial phenotype switching in MITF-low melanoma cell lines. PLoS One. 2017; 12(5):e0177830. PMID: 28545079.
      View in: PubMed
    15. Grelet S, McShane A, Hok E, Tomberlin J, Howe PH, Geslain R. SPOt: A novel and streamlined microarray platform for observing cellular tRNA levels. PLoS One. 2017; 12(5):e0177939. PMID: 28545122.
      View in: PubMed
    16. Ansa-Addo EA, Zhang Y, Yang Y, Hussey GS, Howley BV, Salem M, Riesenberg B, Sun S, Rockey DC, Karvar S, Howe PH, Liu B, Li Z. Membrane-organizing protein moesin controls Treg differentiation and antitumor immunity via TGF-ß signaling. J Clin Invest. 2017 Apr 03; 127(4):1321-1337. PMID: 28287407.
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    17. Lv Z, Rickman KA, Yuan L, Williams K, Selvam SP, Woosley AN, Howe PH, Ogretmen B, Smogorzewska A, Olsen SK. S. pombe Uba1-Ubc15 Structure Reveals a Novel Regulatory Mechanism of Ubiquitin E2 Activity. Mol Cell. 2017 Feb 16; 65(4):699-714.e6. PMID: 28162934.
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    18. Janakiraman H, House RP, Talwar S, Courtney SM, Hazard ES, Hardiman G, Mehrotra S, Howe PH, Gangaraju V, Palanisamy V. Repression of caspase-3 and RNA-binding protein HuR cleavage by cyclooxygenase-2 promotes drug resistance in oral squamous cell carcinoma. Oncogene. 2017 06 01; 36(22):3137-3148. PMID: 27941877.
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    19. Metelli A, Wu BX, Fugle CW, Rachidi S, Sun S, Zhang Y, Wu J, Tomlinson S, Howe PH, Yang Y, Garrett-Mayer E, Liu B, Li Z. Surface Expression of TGFß Docking Receptor GARP Promotes Oncogenesis and Immune Tolerance in Breast Cancer. Cancer Res. 2016 12 15; 76(24):7106-7117. PMID: 27913437.
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    20. Jiang Y, Woosley AN, Howe PH. Disabled-2; an autophagic and apoptotic switch. Cell Cycle. 2016 12 16; 15(24):3319-3320. PMID: 27559620.
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    21. Jiang Y, Woosley AN, Sivalingam N, Natarajan S, Howe PH. Cathepsin-B-mediated cleavage of Disabled-2 regulates TGF-ß-induced autophagy. Nat Cell Biol. 2016 08; 18(8):851-63. PMID: 27398911.
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    22. Heise T, Kota V, Brock A, Morris AB, Rodriguez RM, Zierk AW, Howe PH, Sommer G. The La protein counteracts cisplatin-induced cell death by stimulating protein synthesis of anti-apoptotic factor Bcl2. Oncotarget. 2016 May 17; 7(20):29664-76. PMID: 27105491.
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    23. Link LA, Howley BV, Hussey GS, Howe PH. PCBP1/HNRNP E1 Protects Chromosomal Integrity by Translational Regulation of CDC27. Mol Cancer Res. 2016 07; 14(7):634-46. PMID: 27102006.
      View in: PubMed
    24. Brown AS, Mohanty BK, Howe PH. Identification and characterization of an hnRNP E1 translational silencing motif. Nucleic Acids Res. 2016 07 08; 44(12):5892-907. PMID: 27067543.
      View in: PubMed
    25. Gupta S, Hau AM, Al-Ahmadie HA, Harwalkar J, Shoskes AC, Elson P, Beach JR, Hussey GS, Schiemann WP, Egelhoff TT, Howe PH, Hansel DE. Transforming Growth Factor-ß Is an Upstream Regulator of Mammalian Target of Rapamycin Complex 2-Dependent Bladder Cancer Cell Migration and Invasion. Am J Pathol. 2016 05; 186(5):1351-60. PMID: 26988652.
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    26. Brown AS, Mohanty BK, Howe PH. Computational Identification of Post Translational Modification Regulated RNA Binding Protein Motifs. PLoS One. 2015; 10(9):e0137696. PMID: 26368004.
      View in: PubMed
    27. Hussey GS, Howley BV, Howe PH. Post-transcriptional mapping reveals critical regulators of metastasis. Oncoscience. 2015; 2(10):831-2. PMID: 26682267.
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    28. Howley BV, Hussey GS, Link LA, Howe PH. Translational regulation of inhibin ßA by TGFß via the RNA-binding protein hnRNP E1 enhances the invasiveness of epithelial-to-mesenchymal transitioned cells. Oncogene. 2016 Mar 31; 35(13):1725-35. PMID: 26096938.
      View in: PubMed
    29. Nasarre P, Gemmill RM, Potiron VA, Roche J, Lu X, Barón AE, Korch C, Garrett-Mayer E, Lagana A, Howe PH, Drabkin HA. Neuropilin-2 Is upregulated in lung cancer cells during TGF-ß1-induced epithelial-mesenchymal transition. Cancer Res. 2013 Dec 01; 73(23):7111-21. PMID: 24121493.
      View in: PubMed
    30. Hussey GS, Link LA, Brown AS, Howley BV, Chaudhury A, Howe PH. Establishment of a TGFß-induced post-transcriptional EMT gene signature. PLoS One. 2012; 7(12):e52624. PMID: 23285117.
      View in: PubMed
    31. Jiang Y, He X, Howe PH. Disabled-2 (Dab2) inhibits Wnt/ß-catenin signalling by binding LRP6 and promoting its internalization through clathrin. EMBO J. 2012 May 16; 31(10):2336-49. PMID: 22491013.
      View in: PubMed
    32. Beach JR, Hussey GS, Miller TE, Chaudhury A, Patel P, Monslow J, Zheng Q, Keri RA, Reizes O, Bresnick AR, Howe PH, Egelhoff TT. Myosin II isoform switching mediates invasiveness after TGF-ß-induced epithelial-mesenchymal transition. Proc Natl Acad Sci U S A. 2011 Nov 01; 108(44):17991-6. PMID: 22025714.
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    33. Chaudhury A, Hussey GS, Howe PH. 3'-UTR-mediated post-transcriptional regulation of cancer metastasis: beginning at the end. RNA Biol. 2011 Jul-Aug; 8(4):595-9. PMID: 21654215.
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    34. Hussey G, Chaudhury A, Howe PH. Discovery of a metastatic pathway: implications for future cancer treatment. Future Oncol. 2011 Jun; 7(6):703-5. PMID: 21675832.
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    35. Hussey GS, Chaudhury A, Dawson AE, Lindner DJ, Knudsen CR, Wilce MC, Merrick WC, Howe PH. Identification of an mRNP complex regulating tumorigenesis at the translational elongation step. Mol Cell. 2011 Feb 18; 41(4):419-31. PMID: 21329880.
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    36. Penheiter SG, Singh RD, Repellin CE, Wilkes MC, Edens M, Howe PH, Pagano RE, Leof EB. Type II transforming growth factor-beta receptor recycling is dependent upon the clathrin adaptor protein Dab2. Mol Biol Cell. 2010 Nov 15; 21(22):4009-19. PMID: 20881059.
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    37. Mayorga ME, Dong F, Sundararaman S, Huang Y, Jiang Y, Howe PH, Penn MS. Central role for disabled-2 in mesenchymal stem cardiac protein expression and functional consequences after engraftment in acute myocardial infarction. Stem Cells Dev. 2011 Apr; 20(4):681-93. PMID: 20666606.
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    38. Chaudhury A, Chander P, Howe PH. Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles. RNA. 2010 Aug; 16(8):1449-62. PMID: 20584894.
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    39. Chaudhury A, Hussey GS, Ray PS, Jin G, Fox PL, Howe PH. TGF-beta-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI. Nat Cell Biol. 2010 Mar; 12(3):286-93. PMID: 20154680.
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    40. Chaudhury A, Howe PH. The tale of transforming growth factor-beta (TGFbeta) signaling: a soigné enigma. IUBMB Life. 2009 Oct; 61(10):929-39. PMID: 19787707.
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    41. Jiang Y, Luo W, Howe PH. Dab2 stabilizes Axin and attenuates Wnt/beta-catenin signaling by preventing protein phosphatase 1 (PP1)-Axin interactions. Oncogene. 2009 Aug 20; 28(33):2999-3007. PMID: 19581931.
      View in: PubMed
    42. Wildey GM, Howe PH. Runx1 is a co-activator with FOXO3 to mediate transforming growth factor beta (TGFbeta)-induced Bim transcription in hepatic cells. J Biol Chem. 2009 Jul 24; 284(30):20227-39. PMID: 19494111.
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    43. Ramesh S, Wildey GM, Howe PH. Transforming growth factor beta (TGFbeta)-induced apoptosis: the rise & fall of Bim. Cell Cycle. 2009 Jan 01; 8(1):11-7. PMID: 19106608.
      View in: PubMed
    44. Ramesh S, Qi XJ, Wildey GM, Robinson J, Molkentin J, Letterio J, Howe PH. TGF beta-mediated BIM expression and apoptosis are regulated through SMAD3-dependent expression of the MAPK phosphatase MKP2. EMBO Rep. 2008 Oct; 9(10):990-7. PMID: 18704116.
      View in: PubMed
    45. Jiang Y, Prunier C, Howe PH. The inhibitory effects of Disabled-2 (Dab2) on Wnt signaling are mediated through Axin. Oncogene. 2008 Mar 20; 27(13):1865-75. PMID: 17922036.
      View in: PubMed
    46. Rula ME, Cai KQ, Moore R, Yang DH, Staub CM, Capo-Chichi CD, Jablonski SA, Howe PH, Smith ER, Xu XX. Cell autonomous sorting and surface positioning in the formation of primitive endoderm in embryoid bodies. Genesis. 2007 Jun; 45(6):327-38. PMID: 17506089.
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    47. Bandyopadhyay S, Ashraf MZ, Daher P, Howe PH, DiCorleto PE. HOXA9 participates in the transcriptional activation of E-selectin in endothelial cells. Mol Cell Biol. 2007 Jun; 27(12):4207-16. PMID: 17452460.
      View in: PubMed
    48. Chandrasekharan UM, Siemionow M, Unsal M, Yang L, Poptic E, Bohn J, Ozer K, Zhou Z, Howe PH, Penn M, DiCorleto PE. Tumor necrosis factor alpha (TNF-alpha) receptor-II is required for TNF-alpha-induced leukocyte-endothelial interaction in vivo. Blood. 2007 Mar 01; 109(5):1938-44. PMID: 17068152.
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    49. Qi XJ, Wildey GM, Howe PH. Evidence that Ser87 of BimEL is phosphorylated by Akt and regulates BimEL apoptotic function. J Biol Chem. 2006 Jan 13; 281(2):813-23. PMID: 16282323.
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    50. Hocevar BA, Prunier C, Howe PH. Disabled-2 (Dab2) mediates transforming growth factor beta (TGFbeta)-stimulated fibronectin synthesis through TGFbeta-activated kinase 1 and activation of the JNK pathway. J Biol Chem. 2005 Jul 08; 280(27):25920-7. PMID: 15894542.
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    51. Prunier C, Howe PH. Disabled-2 (Dab2) is required for transforming growth factor beta-induced epithelial to mesenchymal transition (EMT). J Biol Chem. 2005 Apr 29; 280(17):17540-8. PMID: 15734730.
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    52. Prunier C, Hocevar BA, Howe PH. Wnt signaling: physiology and pathology. Growth Factors. 2004 Sep; 22(3):141-50. PMID: 15518237.
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    53. Chandrasekharan UM, Yang L, Walters A, Howe P, DiCorleto PE. Role of CL-100, a dual specificity phosphatase, in thrombin-induced endothelial cell activation. J Biol Chem. 2004 Nov 05; 279(45):46678-85. PMID: 15339908.
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    54. Bayon Y, Ortiz MA, Lopez-Hernandez FJ, Howe PH, Piedrafita FJ. The retinoid antagonist MX781 induces clusterin expression in prostate cancer cells via heat shock factor-1 and activator protein-1 transcription factors. Cancer Res. 2004 Aug 15; 64(16):5905-12. PMID: 15313936.
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    55. Lu T, Burdelya LG, Swiatkowski SM, Boiko AD, Howe PH, Stark GR, Gudkov AV. Secreted transforming growth factor beta2 activates NF-kappaB, blocks apoptosis, and is essential for the survival of some tumor cells. Proc Natl Acad Sci U S A. 2004 May 04; 101(18):7112-7. PMID: 15118089.
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    56. Hocevar BA, Mou F, Rennolds JL, Morris SM, Cooper JA, Howe PH. Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J. 2003 Jun 16; 22(12):3084-94. PMID: 12805222.
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    57. Prunier C, Pessah M, Ferrand N, Seo SR, Howe P, Atfi A. The oncoprotein Ski acts as an antagonist of transforming growth factor-beta signaling by suppressing Smad2 phosphorylation. J Biol Chem. 2003 Jul 11; 278(28):26249-57. PMID: 12732634.
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    58. Wildey GM, Patil S, Howe PH. Smad3 potentiates transforming growth factor beta (TGFbeta )-induced apoptosis and expression of the BH3-only protein Bim in WEHI 231 B lymphocytes. J Biol Chem. 2003 May 16; 278(20):18069-77. PMID: 12637528.
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    59. Hocevar BA, Smine A, Xu XX, Howe PH. The adaptor molecule Disabled-2 links the transforming growth factor beta receptors to the Smad pathway. EMBO J. 2001 Jun 01; 20(11):2789-801. PMID: 11387212.
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    60. Patil S, Wildey GM, Brown TL, Choy L, Derynck R, Howe PH. Smad7 is induced by CD40 and protects WEHI 231 B-lymphocytes from transforming growth factor-beta -induced growth inhibition and apoptosis. J Biol Chem. 2000 Dec 08; 275(49):38363-70. PMID: 10995749.
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    61. Brown TL, Patil S, Howe PH. Analysis of TGF-beta-inducible apoptosis. Methods Mol Biol. 2000; 142:149-67. PMID: 10806621.
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    62. Hocevar BA, Howe PH. Regulation of AP-1 activity by TGF-beta. Methods Mol Biol. 2000; 142:97-108. PMID: 10806616.
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    63. Jin G, Howe PH. Promoter analysis of TGF-beta responsive genes by transient transfection and deletional/mutational analysis. Methods Mol Biol. 2000; 142:79-95. PMID: 10806615.
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    64. Hocevar BA, Howe PH. Analysis of TGF-beta-mediated synthesis of extracellular matrix components. Methods Mol Biol. 2000; 142:55-65. PMID: 10806613.
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    65. Brown TL, Patil S, Cianci CD, Morrow JS, Howe PH. Transforming growth factor beta induces caspase 3-independent cleavage of alphaII-spectrin (alpha-fodrin) coincident with apoptosis. J Biol Chem. 1999 Aug 13; 274(33):23256-62. PMID: 10438500.
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    66. Jin G, Howe PH. Transforming growth factor beta regulates clusterin gene expression via modulation of transcription factor c-Fos. Eur J Biochem. 1999 Jul; 263(2):534-42. PMID: 10406964.
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    67. Hocevar BA, Brown TL, Howe PH. TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J. 1999 Mar 01; 18(5):1345-56. PMID: 10064600.
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    68. Brown TL, Patil S, Basnett RK, Howe PH. Caspase inhibitor BD-fmk distinguishes transforming growth factor beta-induced apoptosis from growth inhibition. Cell Growth Differ. 1998 Oct; 9(10):869-75. PMID: 9790498.
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    69. Hocevar BA, Howe PH. Mechanisms of TGF-beta-induced cell cycle arrest. Miner Electrolyte Metab. 1998; 24(2-3):131-5. PMID: 9525695.
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    70. Jin G, Howe PH. Regulation of clusterin gene expression by transforming growth factor beta. J Biol Chem. 1997 Oct 17; 272(42):26620-6. PMID: 9334243.
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    71. Lee YJ, Han Y, Lu HT, Nguyen V, Qin H, Howe PH, Hocevar BA, Boss JM, Ransohoff RM, Benveniste EN. TGF-beta suppresses IFN-gamma induction of class II MHC gene expression by inhibiting class II transactivator messenger RNA expression. J Immunol. 1997 Mar 01; 158(5):2065-75. PMID: 9036950.
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    72. Chai YC, Howe PH, DiCorleto PE, Chisolm GM. Oxidized low density lipoprotein and lysophosphatidylcholine stimulate cell cycle entry in vascular smooth muscle cells. Evidence for release of fibroblast growth factor-2. J Biol Chem. 1996 Jul 26; 271(30):17791-7. PMID: 8663300.
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    73. Hocevar BA, Howe PH. Isolation and characterization of mutant cell lines defective in transforming growth factor beta signaling. Proc Natl Acad Sci U S A. 1996 Jul 23; 93(15):7655-60. PMID: 8755531.
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    74. Reddy KB, Jin G, Karode MC, Harmony JA, Howe PH. Transforming growth factor beta (TGF beta)-induced nuclear localization of apolipoprotein J/clusterin in epithelial cells. Biochemistry. 1996 May 14; 35(19):6157-63. PMID: 8634259.
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    75. Mal A, Poon RY, Howe PH, Toyoshima H, Hunter T, Harter ML. Inactivation of p27Kip1 by the viral E1A oncoprotein in TGFbeta-treated cells. Nature. 1996 Mar 21; 380(6571):262-5. PMID: 8637577.
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    76. Reddy KB, Karode MC, Harmony AK, Howe PH. Interaction of transforming growth factor beta receptors with apolipoprotein J/clusterin. Biochemistry. 1996 Jan 09; 35(1):309-14. PMID: 8555189.
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    77. Lafont AM, Chai YC, Cornhill JF, Whitlow PL, Howe PH, Chisolm GM. Effect of alpha-tocopherol on restenosis after angioplasty in a model of experimental atherosclerosis. J Clin Invest. 1995 Mar; 95(3):1018-25. PMID: 7883949.
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    78. Reddy KB, Hocevar BA, Howe PH. Inhibition of G1 phase cyclin dependent kinases by transforming growth factor beta 1. J Cell Biochem. 1994 Nov; 56(3):418-25. PMID: 7876335.
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    79. Howe PH, Dobrowolski SF, Reddy KB, Stacey DW. Release from G1 growth arrest by transforming growth factor beta 1 requires cellular ras activity. J Biol Chem. 1993 Oct 05; 268(28):21448-52. PMID: 8407989.
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    80. Devajyothi C, Kalvakolanu I, Babcock GT, Vasavada HA, Howe PH, Ransohoff RM. Inhibition of interferon-gamma-induced major histocompatibility complex class II gene transcription by interferon-beta and type beta 1 transforming growth factor in human astrocytoma cells. Definition of cis-element. J Biol Chem. 1993 Sep 05; 268(25):18794-800. PMID: 8103050.
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    81. Reddy KB, Howe PH. Transforming growth factor beta 1-mediated inhibition of smooth muscle cell proliferation is associated with a late G1 cell cycle arrest. J Cell Physiol. 1993 Jul; 156(1):48-55. PMID: 8391008.
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    82. Longstreet M, Miller B, Howe PH. Loss of transforming growth factor beta 1 (TGF-beta 1)-induced growth arrest and p34cdc2 regulation in ras-transfected epithelial cells. Oncogene. 1992 Aug; 7(8):1549-56. PMID: 1630817.
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    83. Howe PH, Draetta G, Leof EB. Transforming growth factor beta 1 inhibition of p34cdc2 phosphorylation and histone H1 kinase activity is associated with G1/S-phase growth arrest. Mol Cell Biol. 1991 Mar; 11(3):1185-94. PMID: 1996085.
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    84. Howe PH, Cunningham MR, Leof EB. Inhibition of mink lung epithelial cell proliferation by transforming growth factor-beta is coupled through a pertussis-toxin-sensitive substrate. Biochem J. 1990 Mar 01; 266(2):537-43. PMID: 2156499.
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    85. Howe PH, Cunningham MR, Leof EB. Distinct pathways regulate transforming growth factor beta 1-stimulated proto-oncogene and extracellular matrix gene expression. J Cell Physiol. 1990 Jan; 142(1):39-45. PMID: 2153688.
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    86. Pietenpol JA, Howe PH, Cunningham MR, Leof EB. Interferon alpha/beta modulation of growth-factor-stimulated mitogenicity in AKR-2B fibroblasts. J Cell Physiol. 1989 Dec; 141(3):453-60. PMID: 2687295.
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    87. Howe PH, Bascom CC, Cunningham MR, Leof EB. Regulation of transforming growth factor beta 1 action by multiple transducing pathways: evidence for both G protein-dependent and -independent signaling. Cancer Res. 1989 Nov 01; 49(21):6024-31. PMID: 2507140.
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    88. Howe PH, Leof EB. Transforming growth factor beta 1 treatment of AKR-2B cells is coupled through a pertussis-toxin-sensitive G-protein(s). Biochem J. 1989 Aug 01; 261(3):879-86. PMID: 2508623.
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    89. Pledger WJ, Howe PH, Leof EB. The regulation of cell proliferation by serum growth factors. Ann N Y Acad Sci. 1982 Dec 10; 397:1-10. PMID: 6961836.
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