The vast potential of heme in regulating biological processes: A global perspective

Heme Biology: The Secret Life of Heme in Regulating Diverse Biological Processes

Volumn , Issue , 2011, Pages 139-160

  Zhang, Li ^a   Arvey, Aaron ^b   Huynh, Donovan Pham ^a   Leslie, Christina ^b  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84970951387     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1142/9789814287937_0007     Document Type: Chapter

References (124)

1. Hou S, Reynolds MF, Horrigan FT, Heinemann SH, Hoshi T. 2006. Reversible binding of heme to proteins in cellular signal transduction. Acc Chem Res 39: 918-924.
2. Padmanaban G, Venkateswar V, Rangarajan PN. 1989. Haem as a multifunctional regulator. Trends Biochem Sci 14: 492-496.
3. Mense SM, Zhang L. 2006. Heme: A versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res 16: 681-692.
4. Rutherford TR, Clegg JB, Weatherall DJ. 1979. K562 human leukaemic cells synthesise embryonic haemoglobin in response to haemin. Nature 280: 164-165.
5. Zhu Y, Hon T, Zhang L. 1999. Heme initiates changes in the expression of a wide array of genes during the early erythroid differentiation stage. Biochem Biophys Res Commun 258: 87-93.
6. Zhu Y, Hon T, Ye W, Zhang L. 2002. Heme deficiency interferes with the Ras-mitogen-activated protein kinase signaling pathway and expression of a subset of neuronal genes. Cell Growth Differ 13: 431-439.
7. Ye W, Zhang L. 2004. Heme controls the expression of cell cycle regulators and cell growth in HeLa cells. Biochem Biophys Res Commun 315: 546-554.
8. Ye W, Zhang L. 2004. Heme deficiency causes apoptosis but does not increase ROS generation in HeLa cells. Biochem Biophys Res Commun 319: 1065-1071.
9. Sengupta A, Hon T, Zhang L. 2005. Heme deficiency suppresses the expression of key neuronal genes and causes neuronal cell death. Brain Res Mol Brain Res 137: 23-30.
10. Ishii DN, Maniatis GM. 1978. Haemin promotes rapid neurite outgrowth in cultured mouse neuroblastoma cells. Nature 274: 372-374.
11. Tsiftsoglou AS, Tsamadou AI, Papadopoulou LC. 2006. Heme as key regulator of major mammalian cellular functions: Molecular, cellular, and pharmacological aspects. Pharmacol Ther 111: 327-345.
12. Weeks CL, Singh S, Madzelan P, Banerjee R, Spiro TG. 2009. Heme regulation of human cystathionine beta-synthase activity: Insights from fluorescence and Raman spectroscopy. J Am Chem Soc 131: 12809-12816.
13. Yi L, Jenkins PM, Leichert LI, Jakob U, Martens JR, Ragsdale SW. 2009. Heme regulatory motifs in heme oxygenase-2 form a thiol/disulfide redox switch that responds to the cellular redox state. J Biol Chem 284: 20556-20561.
14. Faller M, Matsunaga M, Yin S, Loo JA, Guo F. 2007. Heme is involved in microRNA processing. Nat Struct Mol Biol 14: 23-29.
15. Wang II, Zhou Q, Kesinger JW’, Norris C, Valdez C. 2007. Heme regulates exocrine peptidase precursor genes in zebrafish. Exp Biol Med (Maywood) 232: 1170-1180.
16. Chernova T, Steinert JR, Guerin CJ, Nicotera P, Forsythe ID, Smith AG. 2007. Neurite degeneration induced by heme deficiency mediated via inhibition of NMDA receptor-dependent extracellular signal-regulated kinase 1/2 activation. J Neurosci 27: 8475-8485.
17. Yao X, Balamurugan P, Arvey A, Leslie C, Zhang L. 2010. Heme controls the regulation of protein tyrosine kinases Jak2 and Src. Biochem Biophys Res Commun 403: 30-35.
18. Zhang L, Guarente L. 1995. Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J 14: 313-320.
19. Uma S, Matts RL, Guo Y, White S, Chen JJ. 2000. The N-terminal region of the heme-regulated elF2alpha kinase is an autonomous heme binding domain. Eur J Biochem 267: 498-506.
20. Rafie-Kolpin M, Chefalo PJ, Hussain Z, Hahn J, Uma S, Matts RL, Chen JJ. 2000. Two heme-binding domains of heme-regulated eukaryotic initiation factor-2alpha kinase. N terminus and kinase insertion. J Biol Chem 275: 5171-5178.
21. Hach A, Hon T, Zhang L. 1999. A new class of repression modules is critical for heme regulation of the yeast transcriptional activator Hapl. Mol Cell Biol 19: 4324-4333.
22. Hira S, Tomita T, Matsui T, Igarashi K, Ikeda-Saito M. 2007. Bachl, a heme-dependent transcription factor, reveals presence of multiple heme binding sites with distinct coordination structure. IUBMB Life 59: 542-551.
23. Yang J, Ishimori K, O’Brian MR. 2005. Two heme binding sites are involved in the regulated degradation of the bacterial iron response regulator (Irr) protein. J Biol Chem 280: 7671-7676.
24. Yang J, Sangwan I, Lindemann A, Hauser F, Hennecke H, Fischer HM, O’Brian MR. 2006. Bradyrhizobium japonicum senses iron through the status of haem to regulate iron homeostasis and metabolism. Mol Microbiol 60: 427-437.
25. Hausott B, Kurnaz I, Gajovic S, Klimaschewski L. 2009. Signaling by neuronal tyrosine kinase receptors: Relevance for development and regeneration. Anat Rec (Hoboken) 292: 1976-1985.
26. Hartmann JT, Haap M, Kopp HG, Lipp HP. 2009. Tyrosine kinase inhibitors a review on pharmacology, metabolism and side effects. Curr Drug Metab 10: 470-481.
27. Gentile A, Trusolino L, Comoglio PM. 2008. The Met tyrosine kinase receptor in development and cancer. Cancer Metastasis Rev 27: 85-94.
28. Quimby BB, Dasso M. 2003. The small GTPase Ran: Interpreting the signs. Curr Opin Cell Biol 15: 338-344.
29. Toksoz D, Merdek KD. 2002. The Rho small GTPase: Functions in health and disease. Histol Histopathol 17: 915-927.
30. Weissman B, Knudsen KE. 2009. Hijacking the chromatin remodeling machinery: Impact of SWI/SNF perturbations in cancer. Cancer Res 69: 8223-8230.
31. O’Malley BW, Kumar R. 2009. Nuclear receptor coregulators in cancer biology. Cancer Res 69: 8217-8222.
32. Spiegelman BM, Heinrich R. 2004. Biological control through regulated transcriptional coactivators. Cell 119: 157-167.
33. Castano J, Davalos V, Schwartz S, Arango D 2008. EPH receptors in cancer. Histol Histopathol 23: 1011-1023.
34. Arvanitis D, Davy A. 2008. Eph/ephrin signaling: Networks. Genes Dev 22: 416-429.
35. Egea J, Klein R. 2007. Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol 17: 230-238.
36. Pasquale EB. 2008. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133: 38-52.
37. Belhage B, Hansen GH, Elster L, Schousboe A. 1998. Effects of gamma-aminobutyric acid (GABA) on synaptogenesis and synaptic function. Perspect Dev Neurobiol 5: 235-246.
38. Ragan CL, McKernan RM, Wafford K, Whiting PJ. 1993. gamma-Aminobutyric acid-A (GABA-A) receptor/ion channel complex. Biochem Soc Trans *21 (Pt 3): 622-626.
39. Moult PR. 2009. Neuronal glutamate and GABAA receptor function in health and disease. Biochem Soc Trans 37: 1317-1322.
40. Anwyl R. 2009. Metabotropic glutamate receptor-dependent long-term potentiation. Neuropharmacology 56: 735-740.
41. Chernova T, Nicotera P, Smith AG. 2006. Heme deficiency is associated with senescence and causes suppression of N-methyl-D-aspartate receptor subunits expression in primary cortical neurons. Mol Pharmacol 69: 697-705.
42. Tang M, Xu R, Reynolds MF, Garcia ML, Heinemann SH, Hoshi T. 2003. Haem can bind to and inhibit mammalian calcium-dependent Slol BK channels. Nature 425: 531-535.
43. Mendelsohn J. 2004. EGF receptors as a target for cancer therapy. Trans Am Clin Climatol Assoc 115: 249-253; discussion 53-54.
44. Arteaga CL. 2006. EGF receptor mutations in lung cancer: From humans to mice and maybe back to humans. Cancer Cell 9: 421-423.
45. Yamauchi M, Gotoh N. 2009. Theme: Oncology molecular mechanisms determining the efficacy of EGF receptor-specific tyrosine kinase inhibitors help to identify biomarker candidates. Biomark Med 3: 139-151.
46. Reade CA, Ganti AK. 2009. EGFR targeted therapy in non-small cell lung cancer: Potential role of cetuximab. Biologies 3: 215-224.
47. Beltowski J, Lowicka E. 2009. EGF receptor as a drug target in arterial hypertension. Mini Rev Med Chem 9: 526-538.
48. Miettinen P, Ormio P, Hakonen E, Banerjee M, Otonkoski T. 2008. EGF receptor in pancreatic beta-cell mass regulation. Biochem Soc Trans 36: 280-285.
49. Sequist LV, Lynch TJ. 2008. EGFR tyrosine kinase inhibitors in lung cancer: An evolving story. Annu Rev Med 59: 429-442.
50. Badache A, Goncalves A. 2006. The ErbB2 signaling network as a target for breast cancer therapy. J Mammary Gland Biol Neoplasia 11: 13-25.
51. Melisko ME, Glantz M, Rugo HS. 2009. New challenges and opportunities in the management of brain metastases in patients with ErbB2-positive metastatic breast cancer. Nat Clin Pract Oncol 6: 25-33.
52. Sorkin A, Goh LK. 2009. Endocytosis and intracellular trafficking of ErbBs. Exp Cell Res 315: 683-696.
53. Yu D, Hung MC. 2000. Overexpression of ErbB2 in cancer and ErbB2-targeting strategies. Oncogene 19: 6115-6121.
54. Garratt AN, Ozcelik C, Birchmeier C. 2003. ErbB2 pathways in heart and neural diseases. Trends Cardiovasc Med 13: 80-86.
55. Baselga J, Swain SM. 2009. Novel anticancer targets: Revisiting ERBB2 and discovering ERBB3. Nat Rev Cancer 9: 463-475.
56. Baxter RC, Twigg SM. 2009. Actions of IGF binding proteins and related proteins in adipose tissue. Trends Endocrinol Metab 20: 499-505.
57. Gualco E, Wang JY, Del Valle L, Urbanska K, Peruzzi F, Khalili K, Amini S, Reiss K. 2009. IGF-IR in neuroprotection and brain tumors. Front Biosci 14: 352-375.
58. Tao Y, Pinzi V, Bourhis J, Deutsch E. 2007. Mechanisms of disease: Signaling of the insulin-like growth factor 1 receptor pathway therapeutic perspectives in cancer. Nat Clin Pract Oncol 4: 591-602.
59. LeRoith D, Yakar S. 2007. Mechanisms of disease: Metabolic effects of growth hormone and insulin-like growth factor 1. Nat Clin Pract Endocrinol Metab 3: 302-310.
60. Freude S, Schilbach K, Schubert M. 2009. The role of IGF-1 receptor and insulin receptor signaling for the pathogenesis of Alzheimer’s disease: From model organisms to human disease. Curr Alzheimer Res 6: 213-223.
61. Rowzee AM, Lazzarino DA, Rota L, Sun Z, Wood TL. 2008. IGF ligand and receptor regulation of mammary development. J Mammary Gland Biol Neoplasia 13: 361-370.
62. Abbas A, Grant PJ, Kearney MT. 2008. Role of IGF-1 in glucose regulation and cardiovascular disease. Expert Rev Cardiovasc Ther 6: 1135-1149.
63. Arai Y, Kojima T, Takayama M, Hirose N. 2009. The metabolic syndrome. IGF-1, and insulin action. Mol Cell Endocrinol 299: 124-128.
64. Werner H, Weinstein D, Bentov I. 2008. Similarities and differences between insulin and IGF-I: Structures, receptors, and signalling pathways. Arch Physiol Biochem 114: 17-22.
65. Gilfillan AM, Rivera J. 2009. The tyrosine kinase network regulating mast cell activation. Immunol Rev 228: 149-169.
66. Filippakopoulos P, Midler S, Knapp S. 2009. SH2 domains: Modulators of nonreceptor tyrosine kinase activity. Curr Opin Struct Biol 19: 643-649.
67. Mocsai A, Ruland J, Tybulewicz VL. 2010. The SYK tyrosine kinase: A crucial player in diverse biological functions. Nat Rev Immunol 10: 387-402.
68. Schlessinger J, Lemmon MA. 2003. SH2 and PTB domains in tyrosine kinase signaling. Sci STKE 2003: RE12.
69. Perona R. 2006. Cell signalling: Growth factors and tyrosine kinase receptors. Clin Transl Oncol 8: 77-82.
70. Csiszar A. 2006. Structural and functional diversity of adaptor proteins involved in tyrosine kinase signalling. Bioessays 28: 465-479.
71. Tohyama Y, Yamamura II. 2009. Protein tyrosine kinase, syk: A key player in phagocytic cells. J Biochem 145: 267-273.
72. Constantinescu SN, Girardot M, Pecquet C. 2008. Mining for JAK-STAT mutations in cancer. Trends Biochem Sci 33: 122-131.
73. Guarino M. 2010. Src signaling in cancer invasion. J Cell Physiol 223: 14-26.
74. Fizazi K. 2007. The role of Src in prostate cancer. Ann Oncol 18: 1765-1773.
75. Li S. 2007. Src kinase signaling in leukaemia. Int J Biochem Cell Biol 39: 1483-1488.
76. Verma A, Kambhampati S, Parmar S, Platanias LC. 2003. Jak family of kinases in cancer. Cancer Metastasis Rev 22: 423-434.
77. Lin J, Arlinghaus R. 2008. Activated c-Abl tyrosine kinase in malignant solid tumors. Oncogene 27: 4385-4391.
78. Yim EK, Siwko S, Lin SY. 2009. Exploring Rak tyrosine kinase function in breast cancer. Cell Cycle 8: 2360-2364.
79. Stirewalt DL, Meshinchi S. 2009. Receptor tyrosine kinase alterations in AML — biology and therapy. Cancer Treat Res 145: 85-108.
80. Valentino L, Pierre J. 2006. JAK/STAT signal transduction: Regulators and implication in hematological malignancies. Biochem Pharmacol 71: 713-721.
81. Wagh PK, Peace BE, Waltz SE. 2008. Met-related receptor tyrosine kinase Ron in tumor growth and metastasis. Adv Cancer Res 100: 1-33.
82. Bradshaw JM. 2010. The Src, Syk, and Tec family kinases: Distinct types of molecular switches. Cell Signal 22: 1175-1184.
83. Funakoshi-Tago M, Pelletier S, Moritake H, Parganas E, Ihle JN. 2008. Jak2 FERM domain interaction with the erythropoietin receptor regulates Jak2 kinase activity. Mol Cell Biol 28: 1792-1801.
84. Grote K, Luchtefeld M, Schieffer B. 2005. JANUS under stress role of JAK/STAT signaling pathway in vascular diseases. Vascul Pharmacol 43: 357-363.
85. Haan C, Kreis S, Margue C, Behrmann I. 2006. Jaks and cytokine receptors an intimate relationship. Biochem Pharmacol 72: 1538-1546.
86. Hall T, Emmons TL, Chrencik JE, Gormley JA, Weinberg RA, Leone JW, Hirsch JL, Saabye MJ, Schindler JF, Day JE, Williams JM, Kiefer JR, Lightle SA, Harris MS, Guru S, Fischer HD, Tomasselli AG. 2010. Expression, purification, characterization and crystallization of non- and phosphorylated states of JAK2 and JAK3 kinase domain. Protein Expr Purif 69: 54-63.
87. Igaz P, Toth S, Falus A. 2001. Biological and clinical significance of the JAK-STAT pathway; lessons from knockout mice. Inflamm Res 50: 435-441.
88. Kurdi M, Boas GW. 2009. JAK redux: A second look at the regulation and role of JAKs in the heart. Am J Physiol Heart Circ Physiol 297: H1545-H1556.
89. Rabkin R, Sun DF, Chen Y, Tan J, Schaefer F. 2005. Growth hormone resistance in uremia, a role for impaired JAK/STAT signaling. Pedia.tr Nephrol 20: 313-318.
90. Schindler CW. 2002. Series introduction. JAK-STAT signaling in human disease. J Clin Invest 109: 1133-1137.
91. Scott MJ, Godshall CJ, Cheadle WG. 2002. Jaks, STATs, Cytokines, and Sepsis. Clin Diagn Lab Immunol 9: 1153-1159.
92. Shuai K, Liu B. 2003. Regulation of JAK-STAT signaling in the immune system. Nat Rev Immunol 3: 900-911.
93. Ward AC, Touw I, Yoshimura A. 2000. The Jak-Stat pathway in normal and perturbed hematopoiesis. Blood 95: 19-29.
94. Wilks AF. 2008. The JAK kinases: not just another kinase drug discovery target. Semin Cell Dev Biol 19: 319-328.
95. Yamaoka K, Saharinen P, Pesu M, Holt VE, Silvennoinen O, O’Shea JJ. 2004. The Janus kinases (Jaks). Genome Biol 5: 253.
96. Parganas E, Wang D, Stravopodis D, Topham DJ, Marine JC, Teglund S, Vanin EF, Bodner S, Colamonici OR, van Deursen JM, Grosveld G, Ihle JN. 1998. Jak2 is essential for signaling through a variety of cytokine receptors. Cell 93: 385-395.
97. Neubauer H, Cumano A, Muller M, Wu H, Huffstadt U, Pfeffer K. 1998. Jak2 deficiency defines an essential developmental checkpoint in definitive hematopoiesis. Cell 93: 397-409.
98. Pelletier S, Gingras S, Funakoshi-Tago M, Howell S, Ihle JN. 2006. Two domains of the erythropoietin receptor are sufficient for Jak2 binding/activation and function. Mol Cell Biol 26: 8527-8538.
99. Jamieson CH, Gotlib J, Durocher JA, Chao MP, Mariappan MR, Lay M, Jones C, Zehnder JL, Lilleberg SL, Weissman IL. 2006. The JAK2 V617F mutation occurs in hematopoietic stem cells in polycythemia vera and predisposes toward erythroid differentiation. Proc Natl Acad Sci USA 103: 6224-6229.
100. Kroger N, Badbaran A, Holler E, Hahn J, Kobbe G, Bornhauser M, Reiter A, Zabelina T, Zander AR, Fehse B. 2007. Monitoring of the JAK2-V617F mutation by highly sensitive quantitative real-time PCR after allogeneic stem cell transplantation in patients with myelofibrosis. Blood 109: 1316-1321.
101. Li Z, Xing S, Wang S, Ho WT, Zhao ZJ. 2007. Characterization of a highly effective protein substrate for analysis of JAK2V617F activity. Exp Hematol 35: 1624-1632.
102. Li Z, Xu M, Xing S, Ho WT, Ishii T, Li Q, Fu X, Zhao ZJ. 2007. Erlotinib effectively inhibits JAK2V617F activity and polycythemia vera cell growth. J Biol Chem 282: 3428-3432.
103. Mossuz P, Arlotto M, Hermouet S, Bouamrani A, Lippert E, Girodon F, Dobo I, Vincent P, Cahn JY, Berger F. 2008. Proteomic study of the impact of the JAK2-V617F mutation on the phenotype of essential thrombo-cythemia. Exp Hematol3G: 1642-1647.
104. Olsen R, Dunphy C, O’Malley D, Rice L, Ewton A, Chang C-C. 2008. The implication of identifying JAK2 (V617F) in myeloproliferative neoplasms and myelodysplastic syndromes with bone marrow fibrosis. J Hematopathol 1: 111-117.
105. Williams DM, Kim AH, Rogers O, Spivak JL, Moliterno AR. 2007. Phenotypic variations and new mutations in JAK2 V617F-negative polycythemia vera. erythrocytosis, and idiopathic myelofibrosis. Exp Hematol 35: 1611-1646.
106. Xing S, Wanting TH, Zhao W, Ma J, Wang S, Xu X, Li Q, Fu X, Xu M, Zhao ZJ. 2008. Transgenic expression of JAK2V617F causes myeloproliferative disorders in mice. Blood 111: 5109-5117.
107. Xu X, Zhang Q, Luo J, Xing S, Li Q, Krantz SB, Fu X, Zhao ZJ. 2007. JAK2V617F: Prevalence in a large Chinese hospital population. Blood 109: 339-342.
108. Zhao R, Fu X, Teng L, Li Q, Zhao ZJ. 2003. Blocking the Function of Tyrosine Phosphatase SHP-2 by Targeting Its Src Homology 2 Domains. J Biol Chem 278: 42893-42898.
109. Zhao R, Xing S, Li Z, Fu X, Li Q, Krantz SB, Zhao ZJ. 2005. Identification of an Acquired JAK2 Mutation in Polycythemia Vera. J Biol Chem 280: 22788-22792.
110. Levine RL, Pardanani A, Tefferi A, Gilliland DG. 2007. Role of JAK2 in the pathogenesis and therapy of myeloproliferative disorders. Nat Rev Cancer 7: 673-683.
111. Anderson KE, Sassa S, Bishop DF, Desnick RJ. 2009. Disorders of heme biosynthesis: X-linked sideroblastic anemia and the porphyrias. In The metabolic and molecular bases of inherited disease, ed. CR Scriver, AL Beaudt. WS Sly. D Valle, C Barton, KW Kinzler. B Vogelstein. Chapter 124. pp. 1-53. New York: The McGraw-Hill Companies, Inc.
112. Araujo J, Logothetis C. 2009. Targeting Src signaling in metastatic bone disease. Int J Cancer 124: 1-6.
113. Brunton VG, Frame MC. 2008. Src and focal adhesion kinase as therapeutic targets in cancer. Curr Opin Pharmacol 8: 427-432.
114. Cooper JA, Qian H. 2008. A mechanism for SRC kinase-dependent signaling by noncatalytic receptors. Biochemistry 47: 5681-5688.
115. de Groot J, Milano V. 2009. Improving the prognosis for patients with glioblastoma: The rationale for targeting Src. J Neurooncol 95: 151-163.
116. Finn IIS, 2008. Targeting Src in breast cancer. Ann Oncol ID: 1370-1386.
117. Giaccone G, Zucali PA. 2008. Src as a potential therapeutic target in nonsmall-cell lung cancer. Ann Oncol 19: 1219-1223.
118. Hu G, Minshall RD. 2009. Regulation of transendothelial permeability by Src kinase. Microvasc Res 77: 21-25.
119. Ingley E, 2008. Src family kinases: regulation of their activities, levels and identification of new pathways. Biochim Biophys Acta 1784: 56-65.
120. Lavoie JN, Landry MC, Faure RL, Champagne C. 2010. Src-family kinase signaling, actin-mediated membrane trafficking and organellar dynamics in the control of cell fate: Lessons to be learned from the adenovirus E4orf4 death factor. Cell Signal 22: 1604-1614.
121. Saad F, 2009. Src as a therapeutic target in men with prostate cancer and bone metastases. BJ U Int 103: 434-440.
122. Salmond RJ, Filby A, Qureshi I, Caserta S, Zamoyska R. 2009. T-cell receptor proximal signaling via the Src-family kinases, Lck and Fyn, influences T-cell activation, differentiation, and tolerance. Immunol Rev 228: 9-22.
123. Sandilands E, Frame MC. 2008. Endosomal trafficking of Src tyrosine kinase. Trends Cell Biol 18: 322-329.
124. Seliger B, Massa C, Rini B, Ko J, Finke J. 2010. Antitumour and immune-adjuvant activities of protein-tyrosine kinase inhibitors. Trends Mol Med 16: 184-192.