TWIST activation by hypoxia inducible factor-1 (HIF-1): Implications in metastasis and development

Cell Cycle

Volumn 7, Issue 14, 2008, Pages 2090-2096

  Yang, Muh Hwa ^a,b   Wu, Kou Juey ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

Development; Epithelial mesenchymal transition; HIF 1 ; Metastasis; TWIST

Indexed keywords

CARBONATE DEHYDRATASE IX; CATHEPSIN D; CHEMOKINE RECEPTOR CXCR4; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FIBRONECTIN 1; GELATINASE A; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSYL OXIDASE LIKE 2; MYOD PROTEIN; PROTEIN LYSINE 6 OXIDASE; PROTEIN UPAR; SMAD INTERACTING PROTEIN 1; SMALL INTERFERING RNA; SOMATOMEDIN C; STAT3 PROTEIN; TRANSCRIPTION FACTOR E47; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1; TRASTUZUMAB; UVOMORULIN; VASCULOTROPIN; WNT1 PROTEIN;

ANGIOGENESIS; ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER PATIENT; CANCER RESISTANCE; CARCINOGENESIS; CELL INVASION; CELL METABOLISM; COLON CANCER; EMBRYO DEVELOPMENT; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM; GASTRULATION; GENE FUNCTION; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HYPOXIA; KIDNEY CANCER; LIVER CANCER; LUNG CANCER; MELANOMA; MESENCHYME; MESODERM; METASTASIS; METASTASIS POTENTIAL; NONHUMAN; PROGNOSIS; PROSTATE CANCER; PROTEIN FUNCTION; REGULATORY MECHANISM; STOMACH CANCER; TRANSCRIPTION INITIATION; TUMOR VASCULARIZATION;

GASTROPODA;

EID: 47749131186     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.7.14.6324     Document Type: Article

References (101)

1. Bristow RG, Hill R P. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 2008; 8:180-92.
2. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2002; 2:38-47.
3. Semenza GL, Jiang BH, Leung SW, Passantino R, Concordet J P, Maire P, Giallongo A. Hypoxia response elements in the aldolase A, enolase 1 and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J Biol Chem 1996; 271:32529-37.
4. Wenger RH, Gassmann M. Oxygen(es) and the hypoxia-inducible factor 1. Biol Chem 1997; 378:609-16.
5. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev 1998; 12:149-62.
6. Ryan HE, Lo J, Johnson RS. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J 1998; 17:3005-15.
7. Provot S, Zinyk D, Gunes Y, Kathri R, Le Q, Kronenberg HM, Johnson RS, Longaker MT, Giaccia AJ, Schipani E. Hif-1α regulates differentiation of limb bud mesenchyme and joint development. J Cell Biol 2007; 177:451-64.
8. Maxwell PH. The HIF pathway in cancer. Semin Cell Dev Biol 2005; 16:523-30.
9. Gupta G P, Massague J. Cancer metastasis: building a framework. Cell 2006; 127:679-95.
10. Harris AL. Hypoxia-a key regulatory factor in tumor growth. Nat Rev Cancer 2002; 2:38-47.
11. Semenza GL. HIF-1 and tumor progression: pathophysiology and therapeutics. Trends Mol Med 2002; 8:62-7.
12. Forsythe JA, Jiang BH, Lyer NV, Agani F, Leung SW, Koos RD, Semenza GL. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996; 16:4604-13.
13. Schneider B P, Sledge GW Jr. Drug insight: VEGF as a therapeutic target for breast cancer. Nat Clin Pract Oncol 2007; 4:181-9.
14. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002; 29:15-8
15. Krishnamachary B, Zagzag D, Nagasawa H, Rainey K, Okuyama H, Baek JH, Semenza GL. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal carcinoma mediated by TCF3, ZFHX1A and ZFHX1B. Cancer Res 2006; 66:2725-31.
16. Krishnamachary B, Berg-Dixon S, Kelly B, Agani F, Feldser D, Ferreira G, Iyer N, LaRusch J, Pak B, Taghavi P, Semenza GL. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res 2003; 63:1138-43.
17. Thiery J P. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002; 2:442-54.
18. Higgins D F, Kimura K, Bernhardt WM, Shrimanker N, Akai Y, Hohenstein B, Saito Y, Johnson RS, Kretzler M, Cohen CD, Eckardt KU, Iwano M, Haase VH. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 2007; 117:3810-20.
19. Thompson E W, Newgreen D F. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer Res 2005; 65:5991-5.
20. Thiery J P, Sleeman J P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 2006; 7:131-42.
21. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000; 2:76-83.
22. Hajra KM, Chen DY, Fearon ER. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002; 62:1613-8.
23. Yang J, Mani S, Donaher J, Ramaswamy S, Itzykson R, Come C, Savagner P, Gitelman I, Richardson A, Weinberg R. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004; 117:927-39.
24. Grooteclaes ML, Frisch SM. Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 2000; 19:3823-8.
25. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D, van Roy F. The two-handed E box binding zinc finger protein SIP1 down-regulates E-cadherin and induces invasion. Mol Cell 2001; 7:1267-78.
26. Pérez-Moreno MA, Locascio A, Rodrigo I, Dhondt G, Portillo F, Nieto MA, Cano A. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J Biol Chem 2001; 276:27424-31.
27. Harada H, Kizaka-Kondoh S, Li G, Itasaka S, Shibuya K, Inoue M, Hiraoka M. Significance of HIF-1-active cells in angiogenesis and radioresistance. Oncogene 2007; 26:7508-16.
28. Lundgren K, Holm C, Landberg G. Hypoxia and breast cancer: prognostic and therapeutic implications. Cell Mol Life Sci 2007; 64:3233-47.
29. Vaupel P. The role of hypoxia-induced factors in tumor progression. The Oncologist 2004; 9:10-7.
30. Yang MH, Wu MZ, Chiou SH, Chen PM, Chang SY, Teng SC, Wu KJ. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 2008; 10:295-305.
31. Peinado H, Cano A. A hypoxic twist in metastasis. Nat Cell Biol 2008; 10:253-4.
32. Evans AJ, Russell RC, Roche O, Burry NT, Fish JE, Chow VW, Kim WY, Saravanan A, Maynard MA, Gervais ML, Sufan RI, Roberts AM, Wilson LA, Betten M, Vandewalle C, Berx G, Marsden PA, Irwin MS, The BT, Jewett MA, Ohh M. VHL promotes E2 box-dependent E-cadherin transcription by HIF-mediated regulation of SIP1 and Snail. Mol Cell Biol 2007; 27:157-69.
33. Erler J T, Bennewith EL, Nicolau M, Dornhofer N, Kong C, Le Q T, Chi J T, Jeffrey SS, Giaccia AJ. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 2006; 440:1222-6.
34. Peinado H, Iglesias-de la Cruz MC, Olmeda D, Csiszar K, Fong KSK, Vega S, Nieto MA, Cano A, Portillo F. A molecular role for lyxyl oxidase-like 2 enzyme in Snail regulation and tumor progression. EMBO J 2005; 24:3446-58.
35. 2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 1998; 95:7987-92.
36. Yoshimura H, Dhar DK, Kohno H, Kubota H, Fujii T, Ueda S, Kinugasa S, Tachibana M, Nagasue N. Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression. Clin Cancer Res 2004; 10:8554-60.
37. Koukourakis MI, Bentzen SM, Giatromanolaki A, Wilson GD, Daley FM, Saunders MI, Dische S, Sivridis E, Harris AL. Endogenous markers of two separate hypoxia response pathways (hypoxia inducible factor 2 alpha and carbonic anhydrase 9) are associated with radiotherapy failure in head and neck cancer patients recruited in the CHART randomized trial. J Clin Oncol 2006; 24:727-35.
38. nd chromosome. Roux's Arch Dev Biol 1984; 193:267-82.
39. Castanon I, Baylies MK. Twist in fate: evolutionary comparison of Twist structure and function. Gene 2002; 287:11-22.
40. Furlong EE, Andersen EC, Null B, White K P, Scott M P. Patterns of gene expression during Drosophila mesoderm development. Science 2001; 293:1629-33.
41. Yang J, Mani SA, Weinberg RA. Exploring a new twist on tumor metastasis. Cancer Res 2006; 66:4549-52.
42. Bushdid PB, Brantley DM, Yull FE, Blaeuer GL, Hoffman LH, Niswander L, Kerr LD. Inhibition of NFκB activity results in disruption of the apical ectodermal ridge and aberrant limb morphogenesis. Nature 1998; 392:615-18.
43. Sosic D, Richardson JA, Yu K, Ornitz DM, Olson EN. Twist regulates cytokine gene expression through a negative feedback loop that represses NFkappaB activity. Cell 2003; 112:169-80.
44. Pham CG, Bubici C, Zazzeroni F, Knabb JR, Papa S, Kuntzen C, Franzoso G. Upregulation of Twist-1 by NFκB blocks cytotoxicity induced by chemotherapeutic drugs. Mol Cell Biol 2007; 27:3920-35.
45. Dupont J, Fernandez AM, Glackin CA, Helman L, LeRoith D. Insulin-like growth factor 1 (IGF-1)-induced twist expression is involved in the anti-apoptotic effects of the IGF-1 receptor. J Biol Chem 2001; 276:26699-707.
46. Dong YF, Soung DY, Chang Y, Enomoto-Iwamoto M, Paris M, O'Keefe RJ, Schwarz EM, Dris H. Transforming growth factor-beta and Wnt signals regulate chondrocyte differentiation through Twist1 in a stage-specific manner. Mol Endocrinol 2007; 21:2805-20.
47. Howe LR, Watanabe O, Leonard J, Brown AMC. Twist is upregulated in response to Wnt1 and inhibits mouse mammary cell differentiation. Cancer Res 2003; 63:1906-13.
48. Satoh K, Hamada S, Kimura K, Kanno A, Hirota M, Umino J, Fujibuchi W, Masamune A, Tanaka N, Miura K, Egawa S, Motoi F, Unno M, Vonderhaar BK, Shimosegawa T. Upregulation of MSX2 enhances the malignant phenotype and is associated with twist1 expression in human pancreatic cancer cells. Am J Pathol 2008; 172:926-39.
49. Lo HW, Hsu SC, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via upregulation of TWIST gene expression. Cancer Res 2007; 67:9066-76.
50. Cheng GZ, Zhang W, Sun M, Wang Q, Coppola D, Mansour M, Xu L, Costanzo C, Cheng JQ, Wang LH. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 2008; Epub.
51. Ryan HE, Lo J, Johnson RS. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J 1998; 17:3005-15.
52. Chen Z F, Behringer RR. Twist is required in head mesenchyme for cranial neural tube morphogenesis. Genes Dev 1995; 9:686-99.
53. Ip Y T, Park RE, Kosman D, Yazdanbakhsh K, Levine M. dorsal-twist interactions establish snail expression in the presumptive mesoderm of the Drosophila embryo. Genes Dev 1992; 6:1518-30.
54. Ma L, Teruya-Feldstein J, Weinberg RA. Tumor invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 2007; 449:682-8.
55. Peinado H, Olmedo D, Cano A. Snail, ZEB and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007; 7:415-28.
56. Trastour C, Benizri E, Ettore F, Ramaioli A, Chamorey E, Pouysségur J, Berra E. HIF-1alpha and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. Int J Cancer 2007; 120:1451-8.
57. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI. Hypoxia-inducible factor-2 alpha (HIF-2 alpha) induces angiogenesis in breast carcinomas. Appl Immunohistochem Mol Morphol 2006; 14:78-82
58. Kim SJ, Rabbani ZN, Dewhirst WM , Vujaskovic Z, Vollmer RT, Schreiber EG, Oosterwijk E, Kelley MJ. Expression of HIF-1alpha, CA IX, VEGF and MMP-9 in surgically resected non-small cell lung cancer. Lung Cancer 2005; 49:325-35.
59. Huang GW, Yang LY, Lu WQ. Expression of hypoxia-inducible factor 1alpha and vascular endothelial growth factor in hepatocellular carcinoma: Impact on neovascularization and survival. World J Gastroenterol 2005; 11:1705-8.
60. Saarnio S, Parkkila S, Parkkila AK, Pastoreková S, Haukipuro K, Pastorek J, Juvonen T, Karttunen TJ. Transmembrane carbonic anhydrase, MN/CA IX, is a potential biomarker for biliary tumours. J Hepatol 2001; 35:643-9.
61. Sumiyoshi Y, Kakeji Y, Egashira A, Mizokami K, Orita H, Maehara Y. Overexpression of hypoxia-inducible factor 1alpha and p53 is a marker for an unfavorable prognosis in gastric cancer. Clin Cancer Res 2006; 12:5112-7.
62. Driessen A, Landuyt W, Pastorekova S, Moons J, Goethals L, Haustermans K, Nafteux P, Penninckx F, Geboes K, Lerut T, Ectors N. Expression of carbonic anhydrase IX (CA IX), a hypoxia-related protein, rather than vascular-endothelial growth factor (VEGF), a proangiogenic factor, correlates with an extremely poor prognosis in esophageal and gastric adenocarcinomas. Ann Surg 2006; 243:334-40.
63. Klatte T, Seligson DB, Riggs SB, Leppert JT, Berkman MK, Kleid MD, Yu H, Kabbinavar F F, Pantuck AJ, Belldegrun AS. Hypoxia-inducible factor 1 alpha in clear cell renal cell carcinoma. Clin Cancer Res 2007; 13:7388-93.
64. Boddy JL, Fox SB, Han C, Campo L, Turley H, Kanga S, Malone PR, Harris AL. The androgen receptor is significantly associated with vascular endothelial growth factor and hypoxia sensing via hypoxia-inducible factors HIF-1a, HIF-2a, and the prolyl hydroxylases in human prostate cancer. Clin Cancer Res 2005; 11:7658-63.
65. Giatromanolaki A, Sivridis E, Kouskoukis C, Gatter KC, Harris AL, Koukourakis MI. Hypoxia-inducible factors 1alpha and 2alpha are related to vascular endothelial growth factor expression and a poorer prognosis in nodular malignant melanomas of the skin. Melanoma Res 2003; 13:493-501.
66. Maeda G, Chiba T, Okazaki M, Satoh T, Taya Y, Aoba T, Kato K, Kawashiri S, Imai K. Expression of SIP1 in oral squamous cell carcinomas: implications for E-cadherin expression and tumor progression. Int J Oncol 2005; 27:1535-41.
67. Watanabe O, Imamura H, Shimizu T, Kinoshita J, Okabe T, Hirano A, Yoshimatsu K, Konno S, Aiba M, Ogawa K. Expression of twist and wnt in human breast cancer. Anticancer Res 2004; 24:3851-6.
68. Blanco MJ, Moreno-Bueno G, Sarrio D, Locascio A, Cano A, Palacios J, Nieto MA. Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 2002; 21:3241-6.
69. Elloul S, Elstrand MB, Nesland JM, Tropé CG, Kvalheim G, Goldberg I, Reich R, Davidson B. Snail, Slug and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 2005; 103:1631-43.
70. Shih JY, Tsai MF, Chang TH, Chang YL, Yuan A, Yu CJ, Lin SB, Liou GY, Lee ML, Chen JJ, Hong TM, Yang SC, Su JL, Lee YC, Yang PC. Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin Cancer Res 2005; 11:8070-8.
71. Lee TK, Poon RT, Yuen A P, Ling MT, Kwok WK, Wang XH, Wong YC, Guan XY, Man K, Chau KL, Fan ST. Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition. Clin Cancer Res 2006; 12:5369-76.
72. Sugimachi K, Tanaka S, Kameyama T, Taguchi K, Aishima S, Shimada M, Sugimachi K, Tsuneyoshi M. Transcriptional repressor snail and progression of human hepatocellular carcinoma. Clin Cancer Res 2003; 9:2657-64.
73. Yan-Qi Z, Xue-Yan G, Shuang H, Yu C, Fu-Lin G, Fei-Hu B, Shi-Ren S, Xu-Feng W, Jie-D, Dai-Ming F. Expression and significance of TWIST basic helix-loop-helix protein overexpression in gastric cancer. Pathology 2007; 39:470-5.
74. Rosivatz E, Becker I, Specht K, Fricke E, Luber B, Busch R, Höfler H, Becker K F. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol 2002; 161:1881-91.
75. Alves C, Rosivatz E, Schott C, Hollweck R, Becker I, Sarbia M, Carneiro F, Becker K F. Slug is overexpressed in gastric carcinomas and may act synergistically with SIP1 and Snail in the downregulation of E-cadherin. J Pathol 2007; 211:507-15.
76. Roy HK, Smyrk TC, Koetsier J, Victor TA, Wali RK. The transcriptional repressor SNAIL is overexpressed in human colon cancer. Dig Dis Sci 2005; 50:42-6.
77. Peñ'a C, García JM, García V, Silva J, Domínguez G, Rodríguez R, Maximiano C, García de Herreros A, Muñ'oz A, Bonilla F. The expression levels of the transcriptional regulators p300 and CtBP modulate the correlations between SNAIL, ZEB1, E-cadherin and vitamin D receptor in human colon carcinomas. Int J Cancer 2006; 119:2098-104.
78. Yuen H F, Chua CW, Chan Y P, Wong YC, Wang X, Chan KW. Significance of TWIST and E-cadherin expression in the metastatic progression of prostatic cancer. Histopathology 2007; 50:648-58.
79. Hoek K, Rimm DL, Williams KR, Zhao H, Ariyan S, Lin A, Kluger HM, Berger AJ, Cheng E, Trombetta ES, Wu T, Niinobe M, Yoshikawa K, Hannigan GE, Halaban R. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res 2004; 64:5270-82.
80. Thomson S, Buck E, Petti F, Griffin G, Brown E, Ramnarine N, Iwata KK, Gibson N, Haley JD. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small cell carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res 2005; 65:9455-62.
81. Yauch RL, Januario T, Eberhard DA, Cavet G, Zhu W, Fu L, Pham TQ, Soriano R, Stinson J, Seshagiri S, Modrusan Z, Lin CY, O'Neil V, Amler LC. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clin. Cancer Res 2005; 11:8686-98.
82. Yang AD, Fan F, Camp ER, van Buren G, Liu W, Somcio R, Gray MJ, Cheng H, Hoff PM, Ellis LM. Chronic oxaliplatin resistance induces epithelial-to- mesenchymal transition in colorectal cancer cell lines. Clin Cancer Res 2006; 12:4147-53
83. Cheng GZ, Chan J, Wang Q, Zhang W, Sun CD, Wang LH. Twist transcriptionally upregulates AKT2 in breast cancer cells leading to increased migration, invasion and resistance to paclitaxel. Cancer Res 2007; 67:1979-87.
84. Shiota M, Izumi H, Onitsuka T, Miyamoto N, Kashiwagi E, Kidani A, Yokomizo A, Naito S, Kohno K. Twist promotes tumor cell growth through YB-1 expression. Cancer Res 2008; 68:98-105.
85. Escriva M, Peiro S, Herranz N, Villagrasa P, Dave N, Montserrat-Sentis B, Murray SA, Franci C, Gridley T, Virtanen I, Garcia de Herreros A. Repression of PTEN phosphatase by Snail1 transcriptional factor during gamma radiation-induced apoptosis. Mol Cell Biol 2008; 28:1528-40.
86. Nagata Y, Lan KH, Zhou X, Tan M, Esteva FJ, Sahin AA, Klos KS, Li P, Monia B P, Nguyen NT, Hortobagyi GN, Hung MC, Yu D. PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell 2004; 6:117-27.
87. Ramírez-Bergeron DL, Simon MC. Hypoxia-inducible factor and the development of stem cells of the cardiovascular system. Stem Cells 2001; 19:279-86.
88. Mason SD, Howlett RA, Kim MJ, Olfert IM, Hogan MC, McNulty W, Hickey R P, Wagner PD, Kahn CR, Giordano FJ, Johnson RS. Loss of skeletal muscle HIF-1α results in altered exercise endurance. PLoS Biol 2004; 2:288.
89. Huang Y, Hickey R P, Yeh JL, Liu D, Dadak A, Young LH, Johnson RS, Giordano FJ. Cardiac myocyte-specific HIF-1a deletion alters vascularizatin, energy availability, calcium flux and contractility in the normoxic heart. FASEB J 2004; 18:1138-40.
90. Zinkernagel AS, Johnson RS, Nizet V. Hypoxia inducible factor (HIF) function in innate immunity and infection. J Mol Med 2007; 85:1339-46.
91. Baranova O, Miranda L F, Pichiule P, Dragatsis I, Johnson RS, Chavez JC. Neuron-specific inactivation of the hypoxia inducible factor 1a increases brain injury in a mouse model of transient focal cerebral ischemia. J Neurosci 2007; 27:6320-32.
92. Wang Y, Wan C, Deng L, Liu X, Cao X, Gilbert SR, Bouxsein ML, Faugere MC, Guldberg RE, Gerstenfeld LC, Haase VH, Johnson RS, Schipani E, Clemens TL. The hypoxia-inducible factor 1a pathway couples angiogenesis to osteogenesis during skeletal development. J Clin Invest 2007; 117:1616-26.
93. Schipani E, Ryan HE, Didrickson S, Kobayashi T, Knight M, Johnson RS. Hypoxia in cartilage: HIF-1a is essential for chondrocyte growth arrest and survival. Genes Dev 2001; 15:2865-76.
94. Corsi AK, Kostas SA, Fire A, Krause M. Caenorhabditis elegans twist plays an essential role in non-striated muscle development. Development 2000; 127:2041-51.
95. Sokol NS, Ambros V. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during laval growth. Genes Dev 2005; 19:2343-54.
96. Sandmann T, Girardot C, Brehme M, Tongprasit W, Stolc V, Furlong EE. A core transcrip-tional network for early mesoderm development in Drosophila melanogaster. Genes Dev 2007; 21:436-49
97. Soo K, O'Rourke M P, Khoo PL, Steiner KA, Wong N, Behringer RR, Tam P P. Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev Biol 2002; 247:251-70
98. Rice D P, Aberg T, Chan Y, Tang Z, Kettuneu PJ, Pakarinen L, Maxson RE, Thesleff I. Integration of FGF and TWIST in calvarial bone and suture development. Development 2000; 127:1845-55
99. O'Rourke M P, Tamm P. Twist functions in mouse development. Int J Dev Biol 2002; 46:401-13.
100. Hamamori Y, Wu HY, Satorelli V, Kedes L. The basic domain of myogenic basic helix-loop-helix (bHLH) proteins is the novel target for direct inhibition by another bHLH protein, Twist. Mol Cell Biol 2007; 17:6563-73.
101. Gort EH, van Haaften G, Verlaan I, Groot AJ, Plasterk RH, Shvarts A, Suijkerbuijk K P, van Laar T, van der Wall E, Raman V, van Diest PJ, Tijsterman M, Vooijs M. The TWIST1 oncogene is a direct target of hypoxia-inducible factor-2alpha. Oncogene 2008; 27:1501-10.