The role of hypoxia and exploitation of the hypoxic environment in hematologic malignancies

Molecular Cancer Research

Volumn 12, Issue 10, 2014, Pages 1347-1354

  Muz, Barbara ^a   De La Puente, Pilar ^a   Azab, Feda ^a   Luderer, Micah ^a   Azab, Abdel Kareem ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR; PRODRUG;

ANGIOGENESIS; BONE MARROW; CANCER GROWTH; CANCER RESISTANCE; CARCINOGENESIS; HEMATOLOGIC MALIGNANCY; HUMAN; HYPOXIA; HYPOXIC CELL; METASTASIS; REVIEW; BIOLOGICAL MODEL; CELL HYPOXIA; HEMATOLOGIC NEOPLASMS; MOLECULARLY TARGETED THERAPY; PATHOLOGY; TUMOR MICROENVIRONMENT;

CELL HYPOXIA; HEMATOLOGIC NEOPLASMS; HUMANS; MODELS, BIOLOGICAL; MOLECULAR TARGETED THERAPY; TUMOR MICROENVIRONMENT;

EID: 84907990688     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0028     Document Type: Review

References (83)

1. Krock BL, Skuli N, Simon MC. Hypoxia-induced angiogenesis: good and evil. Genes Cancer 2011;2:1117-33.
2. 2 availability on human cancer. Nat Rev Cancer 2008;8:967-75.
3. Semenza GL, Wang GL. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol Cell Biol 1992;12:5447-54.
4. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001;294:1337-40.
5. Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008;8:851-64.
6. Sanchez A, Tripathy D, Yin X, Desobry K, Martinez J, Riley J, et al. p38 MAPK: a mediator of hypoxia-induced cerebrovascular inflammation. J Alzheimers Dis 2012;32:587-97.
7. Cummins EP, Berra E, Comerford KM, Ginouves A, Fitzgerald KT, Seeballuck F, et al. Prolyl hydroxylase-1 negatively regulates IkappaB kinase-beta, giving insight into hypoxia-induced NFkappaB activity. Proc Natl Acad Sci U S A 2006;103:18154-9.
8. Tafani M, Schito L, Pellegrini L, Villanova L, Marfe G, Anwar T, et al. Hypoxia-increased RAGE and P2 x 7R expression regulates tumor cell invasion through phosphorylation of Erk1/2 and Akt and nuclear translocation of NF-{kappa}B. Carcinogenesis 2011;32:1167-75.
9. Semenza GL. Hypoxia-inducible factors: mediators of cancer progression and targets for cancer therapy. Trends Pharmacol Sci 2012;33:207-14.
10. Grant JL, Smith B. Bone marrow gas tensions, bone marrow blood flow, and erythropoiesis in man. Ann Intern Med 1963;58:801-9.
11. Colla S, Storti P, Donofrio G, Todoerti K, Bolzoni M, Lazzaretti M, et al. Low bone marrow oxygen tension and hypoxia-inducible factor-1alpha overexpression characterize patients with multiple myeloma: role on the transcriptional and proangiogenic profiles of CD138(+) cells. Leukemia 2010;24:1967-70.
12. Sipkins DA, Wei X, Wu JW, Runnels JM, Côté D, Means TK, et al. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005;435:969-73.
13. Levesque JP, Winkler IG, Hendy J, Williams B, Helwani F, Barbier V, et al. Hematopoietic progenitor cell mobilization results in hypoxia with increased hypoxia-inducible transcription factor-1 alpha and vascular endothelial growth factor A in bone marrow. Stem Cells 2007;25:1954-65.
14. Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 2007;104:5431-6.
15. Simsek T, Kocabas F, Zheng J, Deberardinis RJ, Mahmoud AI, Olson EN, et al. The distinct metabolic profi le of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 2010;7:380-90.
16. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971;285:1182-6.
17. Lu X, Kang Y. Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res 2010;16:5928-35.
18. Azab AK, Hu J, Quang P, Azab F, Pitsillides C, Awwad R, et al. Hypoxia promotes dissemination of multiple myeloma through acquisition of epithelial to mesenchymal transition-like features. Blood 2012;119:5782-94.
19. Tannock I. Cell kinetics and chemotherapy: a critical review. Cancer Treat Rep 1978;62:1117-33.
20. Giatromanolaki A, Bai M, Margaritis D, Bourantas KL, Koukourakis MI, Sivridis E, et al. Hypoxia and activated VEGF/receptor pathway in multiple myeloma. Anticancer Res 2010;30:2831-6.
21. Hu Y, Kirito K, Yoshida K, Mitsumori T, Nakajima K, Nozaki Y, et al. Inhibition of hypoxia-inducible factor-1 function enhances the sensitivity of multiple myeloma cells to melphalan. Mol Cancer Ther 2009;8:2329-38.
22. Martin SK, Diamond P, Williams SA, To LB, Peet DJ, Fujii N, et al. Hypoxia-inducible factor-2 is a novel regulator of aberrant CXCL12 expression in multiple myeloma plasma cells. Haematologica 2010;95:776-84.
23. Storti P, Bolzoni M, Donofrio G, Airoldi I, Guasco D, Toscani D, et al. Hypoxia-inducible factor (HIF)-1alpha suppression in myeloma cells blocks tumoral growth in vivo inhibiting angiogenesis and bone destruction. Leukemia 2013;27:1697-706.
24. Hu J, Handisides DR, Van Valckenborgh E, De Raeve H, Menu E, Vande Broek I, et al. Targeting the multiple myeloma hypoxic niche with TH-302, a hypoxia-activated prodrug. Blood 2010;116:1524-7.
25. Passam FH, Alexandrakis MG, Kafousi M, Fotinou M, Darivianaki K, Tsirakis G, et al. Histological expression of angiogenic factors: VEGF, PDGFRalpha, and HIF-1alpha in Hodgkin lymphoma. Pathol Res Pract 2009;205:11-20.
26. Evens AM, Schumacker PT, Helenowski IB, Singh AT, Dokic D, Keswani A, et al. Hypoxia inducible factor-alpha activation in lymphoma and relationship to the thioredoxin family. Br J Haematol 2008;141:676-80.
27. Argyriou P, Papageorgiou SG, Panteleon V, Psyrri A, Bakou V, Pappa V, et al. Hypoxia-inducible factors in mantle cell lymphoma: implication for an activated mTORC1->HIF-1alpha pathway. Ann Hematol 2011;90:315-22.
28. Deeb G, Vaughan MM, McInnis I, Ford LA, Sait SN, Starostik P, et al. Hypoxia-inducible factor-1alpha protein expression is associated with poor survival in normal karyotype adult acute myeloid leukemia. Leuk Res 2011;35:579-84.
29. Wellmann S, Guschmann M, Griethe W, Eckert C, von Stackelberg A, Lottaz C, et al. Activation of the HIF pathway in childhood ALL, prognostic implications of VEGF. Leukemia 2004;18:926-33.
30. Benito J, Shi Y, Szymanska B, Carol H, Boehm I, Lu H, et al. Pronounced hypoxia in models of murine and human leukemia: high efficacy of hypoxia-activated prodrug PR-104. PLoS ONE 2011;6:e23108.
31. Ghosh AK, Shanafelt TD, Cimmino A, Taccioli C, Volinia S, Liu CG, et al. Aberrant regulation of pVHL levels by microRNA promotes the HIF/VEGF axis in CLL B cells. Blood 2009;113:5568-74.
32. Jensen PO, Mortensen BT, Hodgkiss RJ, Iversen PO, Christensen IJ, Helledie N, et al. Increased cellular hypoxia and reduced proliferation of both normal and leukaemic cells during progression of acute myeloid leukaemia in rats. Cell Prolif 2000;33:381-95.
33. Frolova O, Samudio I, Benito JM, Jacamo R, Kornblau SM, Markovic A, et al. Regulation of HIF-1alpha signaling and chemoresistance in acute lymphocytic leukemia under hypoxic conditions of the bone marrow microenvironment. Cancer Biol Ther 2012;13:858-70.
34. Azab AK, Weisberg E, Sahin I, Liu F, Awwad R, Azab F, et al. The influence of hypoxia on CML trafficking through modulation of CXCR4 and E-cadherin expression. Leukemia 2013;27:961-4.
35. de la Puente P, Muz B, Azab F, Azab AK. Cell traffi cking of endothelial progenitor cells in tumor progression. Clin Cancer Res 2013;19:3360-8.
36. Rajkumar SV, Mesa RA, Fonseca R, Schroeder G, Plevak MF, Dispenzieri A, et al. Bone marrow angiogenesis in 400 patients with monoclonal gammopathy of undetermined significance, multiple myeloma, and primary amyloidosis. Clin Cancer Res 2002;8:2210-6.
37. Minoia C, Quero C, Asselti M, Galise I, Marzano AL, Iacobazzi A, et al. Changes in angiogenesis and hypoxia-inducible factor-1alpha protein expression in relapsed/refractory indolent non-Hodgkin lymphomas. Br J Haematol 2013;163:640-5.
38. Dejean E, Renalier MH, Foisseau M, Agirre X, Joseph N, de Paiva GR, et al. Hypoxia-microRNA-16 downregulation induces VEGF expression in anaplastic lymphoma kinase (ALK)-positive anaplastic large-cell lymphomas. Leukemia 2011;25:1882-90.
39. Tadokoro H, Umezu T, Ohyashiki K, Hirano T, Ohyashiki JH. Exosomes derived from hypoxic leukemia cells enhance tube formation in endothelial cells. J Biol Chem 2013;288:34343-51.
40. Dong-Feng Z, Ting L, Cheng C, Xi Z, Xue L, Xing-Hua C, et al. Silencing HIF-1alpha reduces the adhesion and secretion functions of acute leukemia hBMSCs. Braz J Med Biol Res 2012;45:906-12.
41. Yang MH, Wu KJ. TWIST activation by hypoxia inducible factor-1 (HIF-1): implications in metastasis and development. Cell Cycle 2008;7:2090-6.
42. Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA, et al. ERbeta impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 2010;17:319-32.
43. Azab AK, Azab F, Blotta S, Pitsillides CM, Thompson B, Runnels JM, et al. RhoA and Rac1 GTPases play major and differential roles in stromal cell-derived factor-1-induced cell adhesion and chemotaxis in multiple myeloma. Blood 2009;114:619-29.
44. Azab AK, Quang P, Azab F, Pitsillides C, Thompson B, Chonghaile T, et al. P-selectin glycoprotein ligand regulates the interaction of multiple myeloma cells with the bone marrow microenvironment. Blood 2012;119:1468-78.
45. Azab AK, Runnels JM, Pitsillides C, Moreau AS, Azab F, Leleu X, et al. CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 2009;113:4341-4351.
46. Ghobrial IM. Myeloma as a model for the process of metastasis: implications for therapy. Blood 2012;120:20-30.
47. Schelter F, Halbgewachs B, Bäumler P, Neu C, Görlach A, Schrötzlmair F, et al. Tissue inhibitor of metalloproteinases-1-induced scattered liver metastasis is mediated by hypoxia-inducible factor-1alpha. Clin Exp Metastasis 2011;28:91-9.
48. Fiegl M, Samudio I, Clise-Dwyer K, Burks JK, Mnjoyan Z, Andreeff M. CXCR4 expression and biologic activity in acute myeloid leukemia are dependent on oxygen partial pressure. Blood 2009;113:1504-12.
49. Vaupel P, Kelleher DK, Hockel M. Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 2001;28(2 Suppl 8):29-35.
50. Das B, Tsuchida R, Malkin D, Koren G, Baruchel S, Yeger H. Hypoxia enhances tumor stemness by increasing the invasive and tumorigenic side population fraction. Stem Cells 2008;26:1818-30.
51. Cipolleschi MG, Dello Sbarba P, Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem cells. Blood 1993;82:2031-7.
52. Rohwer N, Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat 2011;14:191-201.
53. Axelson H, Fredlund E, Ovenberger M, Landberg G, Pa˚hlman S. Hypoxia-induced dedifferentiation of tumor cells - a mechanism behind heterogeneity and aggressiveness of solid tumors. Semin Cell Dev Biol 2005;16:554-63.
54. Diabira S, Morandi X. Gliomagenesis and neural stem cells: key role of hypoxia and concept of tumor "neo-niche". Med Hypotheses 2008;70:96-104.
55. + sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys 2007;67:1-5.
56. Gustafsson MV, Zheng X, Pereira T, Gradin K, Jin S, Lundkvist J, et al. Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev Cell 2005;9:617-28.
57. Keith B, Simon MC. Hypoxia-inducible factors, stem cells, and cancer. Cell 2007;129:465-72.
58. Tung DC, Chao KS. Targeting hedgehog in cancer stem cells: how a paradigm shift can improve treatment response. Future Oncol 2007;3:569-74.
59. Katoh M. WNT signaling in stem cell biology and regenerative medicine. Curr Drug Targets 2008;9:565-70.
60. Kawano Y, Kikukawa Y, Fujiwara S, Wada N, Okuno Y, Mitsuya H, et al. Hypoxia reduces CD138 expression and induces an immature and stem cell - like transcriptional program in myeloma cells. Int J Oncol 2013;43:1809-16.
61. Wang Y, Liu Y, Malek SN, Zheng P, Liu Y. Targeting HIF1alpha eliminates cancer stem cells in hematological malignancies. Cell Stem Cell 2011;8:399-411.
62. Hernandez-Luna MA, Rocha-Zavaleta L, Vega MI, Huerta-Yepez S. Hypoxia inducible factor-1alpha induces chemoresistance phenotype in non-Hodgkin lymphoma cell line via up-regulation of Bcl-(xL). Leuk Lymphoma 2013;54:1048-55.
63. Zhang H, Li H, Xi HS, Li S. HIF1alpha is required for survival maintenance of chronic myeloid leukemia stem cells. Blood 2012;119:2595-607.
64. Rouault-Pierre K, Lopez-Onieva L, Foster K, Anjos-Afonso F, Lamrissi-Garcia I, Serrano-Sanchez M, et al. HIF-2alpha protects human hematopoietic stem/progenitors and acute myeloid leukemic cells from apoptosis induced by endoplasmic reticulum stress. Cell Stem Cell 2013;13:549-63.
65. He M, Wang QY, Yin QQ, Tang J, Lu Y, Zhou CX, et al. HIF-1alpha downregulates miR-17/20a directly targeting p21 and STAT3: a role in myeloid leukemic cell differentiation. Cell Death Differ 2013;20:408-18.
66. Matsunaga T, Imataki O, Torii E, Kameda T, Shide K, Shimoda H, et al. Elevated HIF-1alpha expression of acute myelogenous leukemia stem cells in the endosteal hypoxic zone may be a cause of minimal residual disease in bone marrow after chemotherapy. Leuk Res 2012;36:e122-4.
67. Rankin EB, Giaccia AJ, Schipani E. A central role for hypoxic signaling in cartilage, bone, and hematopoiesis. Curr Osteoporos Rep 2011;9:46-52.
68. Raje N, Roodman GD. Advances in the biology and treatment of bone disease in multiple myeloma. Clin Cancer Res 2011;17:1278-86.
69. Duan JX, Jiao H, Kaizerman J, Stanton T, Evans JW, Lan L, et al. Potent and highly selective hypoxia-activated achiral phosphoramidate mustards as anticancer drugs. J Med Chem 2008;51:2412-20.
70. Brown JM. Clinical trials of radiosensitizers: what should we expect? Int J Radiat Oncol Biol Phys 1984;10:425-9.
71. Patterson LH. Bioreductively activated antitumor N-oxides: the case of AQ4N, a unique approach to hypoxia-activated cancer chemotherapy. Drug Metab Rev 2002;34:581-92.
72. Albertella MR, Loadman PM, Jones PH, Phillips RM, Rampling R, Burnet N, et al. Hypoxia-selective targeting by the bioreductive prodrug AQ4N in patientswith solid tumors: results of a phase I study. Clin Cancer Res 2008;14:1096-104.
73. Tredan O, Garbens AB, Lalani AS, Tannock IF. The hypoxia-activated ProDrug AQ4N penetrates deeply in tumor tissues and complements the limited distribution of mitoxantrone. Cancer Res 2009;69:940-7.
74. von Pawel J, von Roemeling R, Gatzemeier U, Boyer M, Elisson LO, Clark P, et al. Tirapazamine plus cisplatin versus cisplatin in advanced non-small-cell lung cancer: a report of the international CATAPULT I study group. Cisplatin and tirapazamine in subjects with advanced previously untreated non-small-cell lung tumors. J Clin Oncol 2000;18:1351-9.
75. Hu J, Van Valckenborgh E, Xu D, Menu E, De Raeve H, De Bryune E, et al. Synergistic induction of apoptosis in multiple myeloma cells by bortezomib and hypoxia-activated prodrug TH-302, in vivo and in vitro. Mol Cancer Ther 2013;12:1763-73.
76. Meng F, Evans JW, Bhupathi D, Banica M, Lan L, Lorente G, et al. Molecular and cellular pharmacology of the hypoxia-activated prodrug TH-302. Mol Cancer Ther 2012;11:740-51.
77. Liu Q, Sun JD, Wang J, Ahluwalia D, Baker AF, Cranmer LD, et al. TH-302, a hypoxia-activated prodrug with broad in vivo preclinical combination therapy efficacy: optimization of dosing regimens and schedules. Cancer Chemother Pharmacol 2012;69:1487-98.
78. Patterson AV, Ferry DM, Edmunds SJ, Gu Y, Singleton RS, Patel K, et al. Mechanism of action and preclinical antitumor activity of the novel hypoxia-activated DNA cross-linking agent PR-104. Clin Cancer Res 2007;13:3922-32.
79. McKeage MJ, Gu Y, Wilson WR, Hill A, Amies K, Melink TJ, et al. A phase I trial of PR-104, a pre-prodrug of the bioreductive prodrug PR-104A, given weekly to solid tumour patients. BMC Cancer 2011;11:432.
80. Portwood S, Lal D, Hsu YC, Vargas R, Johnson MK, Wetzler M, et al. Activity of the hypoxia-activated prodrug, TH-302, in preclinical human acute myeloid leukemia (AML) models. Clin Cancer Res 2013;19:6506-19.
81. Yi CYA, Borthakur G, Thall PF. Final report of phase I/II study of PR104, a hypoxia-activated pro-drug, in relapsed/refractory acute leukemia 2013 J Clin Oncol 31, 2013 (suppl; abstr 7074).
82. Zhang H, Qian DZ, Tan YS, Lee K, Gao P, Ren YR, et al. Digoxin and other cardiac glycosides inhibit HIF-1alpha synthesis and block tumor growth. Proc Natl Acad Sci U S A 2008;105:19579-86.
83. Lee KE, Simon MC. From stem cells to cancer stem cells: HIF takes the stage. Curr Opin Cell Biol 2012;24:232-5.