Midkine in the pathology of cancer, neural disease, and inflammation

Pathology International

Volumn 62, Issue 7, 2012, Pages 445-455

  Sakamoto, Kazuma ^a   Kadomatsu, Kenji ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Epithelial mesenchymal interaction transition; Midkine; Nervous system; Renin angiotensin system

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; CELL SURFACE PROTEOGLYCAN; INTEGRIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; MIDKINE; NOTCH2 RECEPTOR; PROTEOGLYCAN; UNCLASSIFIED DRUG;

BLOOD PRESSURE REGULATION; CARCINOGENESIS; GENE; GENE STRUCTURE; HOST RESISTANCE; HUMAN; INFLAMMATION; MIDKINE GENE; NEUROLOGIC DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; EPITHELIAL-MESENCHYMAL TRANSITION; GENE SILENCING; HUMANS; INFLAMMATION; MICE; MOLECULAR SEQUENCE DATA; NEOPLASMS; NERVE GROWTH FACTOR; NERVOUS SYSTEM DISEASES; TUMOR MARKERS, BIOLOGICAL;

EID: 84862856362     PISSN: 13205463     EISSN: 14401827     Source Type: Journal    
DOI: 10.1111/j.1440-1827.2012.02815.x     Document Type: Review

References (121)

1. Hunter T. Signaling-2000 and beyond. Cell 2000; 100: 113-27.
2. Crowley C, Spencer SD, Nishimura MC etal. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 1994; 76: 1001-11.
3. Muramatsu T. Midkine and pleiotrophin: Two related proteins involved in development, survival, inflammation and tumorigenesis. J Biochem (Tokyo) 2002; 132: 359-71.
4. Kadomatsu K, Muramatsu T. Midkine and pleiotrophin in neural development and cancer. Cancer Lett 2004; 204: 127-43.
5. Jacob F. Mouse teratocarcinoma and embryonic antigens. Immunol Rev 1977; 33: 3-32.
6. Kadomatsu K, Tomomura M, Muramatsu T. cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem Biophys Res Commun 1988; 151: 1312-8.
7. Tomomura M, Kadomatsu K, Matsubara S, Muramatsu T. A retinoic acid-responsive gene, MK, found in the teratocarcinoma system. Heterogeneity of the transcript and the nature of the translation product. J Biol Chem 1990; 265: 10765-70.
8. Kadomatsu K, Huang RP, Suganuma T, Murata F, Muramatsu T. A retinoic acid responsive gene MK found in the teratocarcinoma system is expressed in spatially and temporally controlled manner during mouse embryogenesis. J Cell Biol 1990; 110: 607-16.
9. Kaname T, Kuwano A, Murano I, Uehara K, Muramatsu T, Kajii T. Midkine gene (MDK), a gene for prenatal differentiation and neuroregulation, maps to band 11p11.2 by fluorescence in situ hybridization. Genomics 1993; 17: 514-5.
10. Matsubara S, Tomomura M, Kadomatsu K, Muramatsu T. Structure of a retinoic acid-responsive gene, MK, which is transiently activated during the differentiation of embryonal carcinoma cells and the mid-gestation period of mouse embryogenesis. J Biol Chem 1990; 265: 9441-3.
11. Uehara K, Matsubara S, Kadomatsu K, Tsutsui J, Muramatsu T. Genomic structure of human midkine (MK), a retinoic acid-responsive growth/differentiation factor. J Biochem (Tokyo) 1992; 111: 563-7.
12. Pedraza C, Matsubara S, Muramatsu T. A retinoic acid-responsive element in human midkine gene. J Biochem (Tokyo) 1995; 117: 845-9.
13. Adachi Y, Matsubara S, Pedraza C etal. Midkine as a novel target gene for the Wilms' tumor suppressor gene (WT1). Oncogene 1996; 13: 2197-203.
14. Li YS, Milner PG, Chauhan AK etal. Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science 1990; 250: 1690-94.
15. Deuel TF, Zhang N, Yeh HJ, Silos-Santiago I, Wang ZY. Pleiotrophin: A cytokine with diverse functions and a novel signaling pathway. Arch Biochem Biophys 2002; 397: 162-71.
16. Iwasaki W, Nagata K, Hatanaka H etal. Solution structure of midkine, a new heparin-binding growth factor. EMBO J 1997; 16: 6936-46.
17. Akhter S, Ichihara-Tanaka K, Kojima S etal. Clusters of basic amino acids in midkine: Roles in neurite-promoting activity and plasminogen activator-enhancing activity. J Biochem (Tokyo) 1998; 123: 1127-36.
18. Asai T, Watanabe K, Ichihara-Tanaka K etal. Identification of heparin-binding sites in midkine and their role in neurite-promotion. Biochem Biophys Res Commun 1997; 236: 66-70.
19. Englund C, Birve A, Falileeva L, Grabbe C, Palmer RH. Miple1 and miple2 encode a family of MK/PTN homologues in Drosophila melanogaster. Dev Genes Evol 2006; 216: 10-18.
20. Mahoney SA, Perry M, Seddon A, Bohlen P, Haynes L. Transglutaminase forms midkine homodimers in cerebellar neurons and modulates the neurite-outgrowth response. Biochem Biophys Res Commun 1996; 224: 147-52.
21. Kojima S, Inui T, Muramatsu H etal. Dimerization of midkine by tissue transglutaminase and its functional implication. J Biol Chem 1997; 272: 9410-16.
22. Kaname T, Kadomatsu K, Aridome K etal. The expression of truncated MK in human tumors. Biochem Biophys Res Commun 1996; 219: 256-60.
23. Miyashiro I, Kaname T, Nakayama T etal. Expression of truncated midkine in human colorectal cancers. Cancer Lett 1996; 106: 287-91.
24. Miyashiro I, Kaname T, Shin E etal. Midkine expression in human breast cancers: Expression of truncated form. Breast Cancer Res Treat 1997; 43: 1-6.
25. Paul S, Mitsumoto T, Asano Y, Kato S, Kato M, Shinozawa T. Detection of truncated midkine in Wilms' tumor by a monoclonal antibody against human recombinant truncated midkine. Cancer Lett 2001; 163: 245-51.
26. Stoica GE, Kuo A, Powers C etal. Midkine binds to anaplastic lymphoma kinase (ALK) and acts as a growth factor for different cell types. J Biol Chem 2002; 277: 35990-98.
27. Lorente M, Torres S, Salazar M etal. Stimulation of ALK by the growth factor midkine renders glioma cells resistant to autophagy-mediated cell death. Autophagy 2011; 7: 1071-3.
28. Reiff T, Huber L, Kramer M, Delattre O, Janoueix-Lerosey I, Rohrer H. Midkine and Alk signaling in sympathetic neuron proliferation and neuroblastoma predisposition. Development 2011; 138: 4699-708.
29. Muramatsu H, Zou K, Sakaguchi N, Ikematsu S, Sakuma S, Muramatsu T. LDL receptor-related protein as a component of the midkine receptor. Biochem Biophys Res Commun 2000; 270: 936-41.
30. Chen S, Bu G, Takei Y etal. Midkine and LDL-receptor-related protein 1 contribute to the anchorage-independent cell growth of cancer cells. J Cell Sci 2007; 120: 4009-15.
31. Sakamoto K, Bu G, Chen S etal. Premature ligand-receptor interaction during biosynthesis limits the production of growth factor midkine and its receptor LDL receptor-related protein 1. J Biol Chem 2011; 286: 8405-13.
32. Shibata Y, Muramatsu T, Hirai M etal. Nuclear targeting by the growth factor midkine. Mol Cell Biol 2002; 22: 6788-96.
33. Muramatsu H, Zou P, Suzuki H etal. Alpha4beta1- and alpha6beta1-integrins are functional receptors for midkine, a heparin-binding growth factor. J Cell Sci 2004; 117: 5405-15.
34. Huang Y, Hoque MO, Wu F, Trink B, Sidransky D, Ratovitski EA. Midkine induces epithelial-mesenchymal transition through Notch2/Jak2-Stat3 signaling in human keratinocytes. Cell Cycle 2008; 7: 1613-22.
35. Güngör C, Zander H, Effenberger KE etal. Notch signaling activated by replication stress-induced expression of midkine drives epithelial-mesenchymal transition and chemoresistance in pancreatic cancer. Cancer Res 2011; 71: 5009-19.
36. Maeda N, Ichihara-Tanaka K, Kimura T, Kadomatsu K, Muramatsu T, Noda M. A receptor-like protein-tyrosine phosphatase PTPzeta/RPTPbeta binds a heparin-binding growth factor midkine. Involvement of arginine 78 of midkine in the high affinity binding to PTPzeta. J Biol Chem 1999; 274: 12474-9.
37. Kurosawa N, Chen GY, Kadomatsu K, Ikematsu S, Sakuma S, Muramatsu T. Glypican-2 binds to midkine: The role of glypican-2 in neuronal cell adhesion and neurite outgrowth. Glycoconj J 2001; 18: 499-507.
38. Ichihara-Tanaka K, Oohira A, Rumsby M, Muramatsu T. Neuroglycan C is a novel midkine receptor involved in process elongation of oligodendroglial precursor-like cells. J Biol Chem 2006; 281: 30857-64.
39. Morris SW, Kirstein MN, Valentine MB etal. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 1994; 263: 1281-4.
40. Soda M, Choi YL, Enomoto M etal. Identification of the transforming EML4-ALK fusion gene in non-small-cell lung cancer. Nature 2007; 448: 561-6.
41. Chen Y, Takita J, Choi YL etal. Oncogenic mutations of ALK kinase in neuroblastoma. Nature 2008; 455: 971-4.
42. Herz J, Beffert U. Apolipoprotein E receptors: Linking brain development and Alzheimer's disease. Nat Rev Neurosci 2000; 1: 51-8.
43. Suzuki N, Shibata Y, Urano T, Murohara T, Muramatsu T, Kadomatsu K. Proteasomal degradation of the nuclear targeting growth factor midkine. J Biol Chem 2004; 279: 17785-91.
44. Dai LC, Shao JZ, Min LS, Xiao YT, Xiang LX, Ma ZH. Midkine accumulated in nucleolus of HepG2 cells involved in rRNA transcription. World J Gastroenterol 2008; 14: 6249-53.
45. Ueoka C, Kaneda N, Okazaki I, Nadanaka S, Muramatsu T, Sugahara K. Neuronal cell adhesion, mediated by the heparin-binding neuroregulatory factor midkine, is specifically inhibited by chondroitin sulfate E. Structural and functional implications of the over-sulfated chondroitin sulfate. J Biol Chem 2000; 275: 37407-13.
46. Qi M, Ikematsu S, Maeda N etal. Haptotactic migration induced by midkine. Involvement of protein-tyrosine phosphatase zeta. Mitogen-activated protein kinase, and phosphatidylinositol 3-kinase. J Biol Chem 2001; 276: 15868-75.
47. Muramatsu T, Muramatsu H, Kaneda N, Sugahara K. Recognition of glycosaminoglycans by midkine. Methods Enzymol 2003; 363: 365-76.
48. Koide N, Hada H, Shinji T etal. Expression of the midkine gene in human hepatocellular carcinomas. Hepatogastroenterology 1999; 46: 3189-96.
49. Konishi N, Nakamura M, Nakaoka S etal. Immunohistochemical analysis of midkine expression in human prostate carcinoma. Oncology 1999; 57: 253-7.
50. Maeda S, Shinchi H, Kurahara H etal. Clinical significance of midkine expression in pancreatic head carcinoma. Br J Cancer 2007; 97: 405-11.
51. Mishima K, Asai A, Kadomatsu K etal. Increased expression of midkine during the progression of human astrocytomas. Neurosci Lett 1997; 233: 29-32.
52. Moon HS, Park WI, Sung SH, Choi EA, Chung HW, Woo BH. Immunohistochemical and quantitative competitive PCR analyses of midkine and pleiotrophin expression in cervical cancer. Gynecol Oncol 2003; 88: 289-97.
53. Nakagawara A, Milbrandt J, Muramatsu T etal. Differential expression of pleiotrophin and midkine in advanced neuroblastomas. Cancer Res 1995; 55: 1792-7.
54. Ohhashi S, Ohuchida K, Mizumoto K etal. Midkine mRNA is overexpressed in pancreatic cancer. Dig Dis Sci 2009; 54: 811-5.
55. Ren YJ, Zhang QY. Expression of midkine and its clinical significance in esophageal squamous cell carcinoma. World J Gastroenterol 2006; 12: 2006-10.
56. Tsutsui J, Kadomatsu K, Matsubara S etal. A new family of heparin-binding growth/differentiation factors: Increased midkine expression in Wilms' tumor and other human carcinomas. Cancer Res 1993; 53: 1281-5.
57. Xu Y, Qu X, Zhang X etal. Midkine positively regulates the proliferation of human gastric cancer cells. Cancer Lett 2009; 279: 137-44.
58. Ye C, Qi M, Fan QW etal. Expression of midkine in the early stage of carcinogenesis in human colorectal cancer. Br J Cancer 1999; 79: 179-84.
59. O'Brien T, Cranston D, Fuggle S, Bicknell R, Harris AL. The angiogenic factor midkine is expressed in bladder cancer, and overexpression correlates with a poor outcome in patients with invasive cancers. Cancer Res 1996; 56: 2515-8.
60. Ikematsu S, Nakagawara A, Nakamura Y etal. Correlation of elevated level of blood midkine with poor prognostic factors of human neuroblastomas. Br J Cancer 2003; 88: 1522-6.
61. Ikematsu S, Nakagawara A, Nakamura Y etal. Plasma midkine level is a prognostic factor for human neuroblastoma. Cancer Sci 2008; 99: 2070-74.
62. Kaifi JT, Fiegel HC, Rafnsdottir SL etal. Midkine as a prognostic marker for gastrointestinal stromal tumors. J Cancer Res Clin Oncol 2007; 133: 431-5.
63. Ikematsu S, Yano A, Aridome K etal. Serum midkine levels are increased in patients with various types of carcinomas. Br J Cancer 2000; 83: 701-6.
64. Obata Y, Kikuchi S, Lin Y etal. Serum midkine concentrations and gastric cancer. Cancer Sci 2005; 96: 54-6.
65. Jia HL, Ye QH, Qin LX etal. Gene expression profiling reveals potential biomarkers of human hepatocellular carcinoma. Clin Cancer Res 2007; 13: 1133-9.
66. Ota K, Fujimori H, Ueda M etal. Midkine as a prognostic biomarker in oral squamous cell carcinoma. Br J Cancer 2008; 99: 655-62.
67. Ibusuki M, Fujimori H, Yamamoto Y etal. Midkine in plasma as a novel breast cancer marker. Cancer Sci 2009; 100: 1735-9.
68. Maris JM, Matthay KK. Molecular biology of neuroblastoma. J Clin Oncol 1999; 17: 2264-79.
69. Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet 2007; 369: 2106-20.
70. Kadomatsu K, Hagihara M, Akhter S, Fan QW, Muramatsu H, Muramatsu T. Midkine induces the transformation of NIH3T3 cells. Br J Cancer 1997; 75: 354-9.
71. Ratovitski EA, Burrow CR. Midkine stimulates Wilms' tumor cell proliferation via its signaling receptor. Cell Mol Biol (Noisy-le-grand) 1997; 43: 425-31.
72. Ratovitski EA, Kotzbauer PT, Milbrandt J, Lowenstein CJ, Burrow CR. Midkine induces tumor cell proliferation and binds to a high affinity signaling receptor associated with JAK tyrosine kinases. J Biol Chem 1998; 273: 3654-60.
73. Qi M, Ikematsu S, Ichihara-Tanaka K, Sakuma S, Muramatsu T, Kadomatsu K. Midkine rescues Wilms' tumor cells from cisplatin-induced apoptosis: Regulation of Bcl-2 expression by Midkine. J Biochem. 2000; 127: 269-77.
74. Tong Y, Mentlein R, Buhl R etal. Overexpression of midkine contributes to anti-apoptotic effects in human meningiomas. J Neurochem 2007; 100: 1097-107.
75. Choudhuri R, Zhang HT, Donnini S, Ziche M, Bicknell R. An angiogenic role for the neurokines midkine and pleiotrophin in tumorigenesis. Cancer Res 1997; 57: 1814-9.
76. Kojima S, Muramatsu H, Amanuma H, Muramatsu T. Midkine enhances fibrinolytic activity of bovine endothelial cells. J Biol Chem 1995; 270: 9590-96.
77. Takei Y, Kadomatsu K, Matsuo S etal. Antisense oligodeoxynucleotide targeted to Midkine, a heparin-binding growth factor, suppresses tumorigenicity of mouse rectal carcinoma cells. Cancer Res 2001; 61: 8486-91.
78. Takei Y, Kadomatsu K, Goto T, Muramatsu T. Combinational antitumor effect of siRNA against midkine and paclitaxel on growth of human prostate cancer xenografts. Cancer 2006; 107: 864-73.
79. Maehara H, Kaname T, Yanagi K etal. Midkine as a novel target for antibody therapy in osteosarcoma. Biochem Biophys Res Commun 2007; 358: 757-62.
80. Adachi Y, Reynolds PN, Yamamoto M etal. Midkine promoter-based adenoviral vector gene delivery for pediatric solid tumors. Cancer Res 2000; 60: 4305-10.
81. Tomizawa M, Yu L, Wada A etal. A promoter region of the midkine gene that is frequently expressed in human hepatocellular carcinoma can activate a suicide gene as effectively as the alpha-fetoprotein promoter. Br J Cancer 2003; 89: 1086-90.
82. Yu L, Yamamoto N, Kadomatsu K etal. Midkine promoter can mediate transcriptional activation of a fused suicide gene in a broader range of human breast cancer compared with c-erbB-2 promoter. Oncology 2004; 66: 143-9.
83. Matsumoto K, Wanaka A, Takatsuji K, Muramatsu H, Muramatsu T, Tohyama M. A novel family of heparin-binding growth factors, pleiotrophin and midkine, is expressed in the developing rat cerebral cortex. Brain Res Dev Brain Res 1994; 79: 229-41.
84. Nakamura E, Kadomatsu K, Yuasa S etal. Disruption of the midkine gene (Mdk) resulted in altered expression of a calcium binding protein in the hippocampus of infant mice and their abnormal behaviour. Genes Cells 1998; 3: 811-22.
85. Rauvala H, Peng HB. HB-GAM (heparin-binding growth-associated molecule) and heparin-type glycans in the development and plasticity of neuron-target contacts. Prog Neurobiol 1997; 52: 127-44.
86. Kaneda N, Talukder AH, Nishiyama H, Koizumi S, Muramatsu T. Midkine, a heparin-binding growth/differentiation factor, exhibits nerve cell adhesion and guidance activity for neurite outgrowth in vitro. J Biochem (Tokyo) 1996; 119: 1150-56.
87. Owada K, Sanjo N, Kobayashi T etal. Midkine inhibits caspase-dependent apoptosis via the activation of mitogen-activated protein kinase and phosphatidylinositol 3-kinase in cultured neurons. J Neurochem 1999; 73: 2084-92.
88. Sakaguchi N, Muramatsu H, Ichihara-Tanaka K etal. Receptor-type protein tyrosine phosphatase zeta as a component of the signaling receptor complex for midkine-dependent survival of embryonic neurons. Neurosci Res 2003; 45: 219-24.
89. Michikawa M, Kikuchi S, Muramatsu H, Muramatsu T, Kim SU. Retinoic acid responsive gene product, midkine, has neurotrophic functions for mouse spinal cord and dorsal root ganglion neurons in culture. J Neurosci Res 1993; 35: 530-39.
90. Yoshida Y, Goto M, Tsutsui J etal. Midkine is present in the early stage of cerebral infarct. Brain Res Dev Brain Res 1995; 85: 25-30.
91. Wang S, Yoshida Y, Goto M etal. Midkine exists in astrocytes in the early stage of cerebral infarction. Brain Res Dev Brain Res 1998; 106: 205-9.
92. Yoshida Y, Ikematsu S, Moritoyo T etal. Intraventricular administration of the neurotrophic factor midkine ameliorates hippocampal delayed neuronal death following transient forebrain ischemia in gerbils. Brain Res 2001; 894: 46-55.
93. Takada J, Ooboshi H, Ago T etal. Postischemic gene transfer of midkine, a neurotrophic factor, protects against focal brain ischemia. Gene Ther 2005; 12: 487-93.
94. Kim YB, Ryu JK, Lee HJ etal. Midkine, heparin-binding growth factor, blocks kainic acid-induced seizure and neuronal cell death in mouse hippocampus. BMC Neurosci 2010; 11: 42.
95. Unoki K, Ohba N, Arimura H, Muramatsu H, Muramatsu T. Rescue of photoreceptors from the damaging effects of constant light by midkine, a retinoic acid-responsive gene product. Invest Ophthalmol Vis Sci 1994; 35: 4063-8.
96. Sakakima H, Yoshida Y, Muramatsu T etal. Traumatic injury-induced midkine expression in the adult rat spinal cord during the early stage. J Neurotrauma 2004; 21: 471-7.
97. Sakakima H, Yoshida Y, Yamazaki Y etal. Disruption of the midkine gene (Mdk) delays degeneration and regeneration in injured peripheral nerve. J Neurosci Res 2009; 87: 2908-15.
98. Yasuhara O, Muramatsu H, Kim SU, Muramatsu T, Maruta H, McGeer PL. Midkine, a novel neurotrophic factor, is present in senile plaques of Alzheimer disease. Biochem Biophys Res Commun 1993; 192: 246-51.
99. Yu GS, Hu J, Nakagawa H. Inhibition of beta-amyloid cytotoxicity by midkine. Neurosci Lett 1998; 254: 125-8.
100. Muramatsu H, Yokoi K, Chen L, Ichihara-Tanaka K, Kimura T, Muramatsu T. Midkine as a factor to counteract the deposition of amyloid β-peptide plaques: In vitro analysis and examination in knockout mice. Int Arch Med 2011; 4: 1.
101. Bauer J, Strauss S, Schreiter-Gasser U etal. Interleukin-6 and alpha-2-macroglobulin indicate an acute-phase state in Alzheimer's disease cortices. FEBS Lett 1991; 285: 111-4.
102. Namba Y, Tomonaga M, Kawasaki H, Otomo E, Ikeda K. Apolipoprotein E immunoreactivity in cerebral amyloid deposits and neurofibrillary tangles in Alzheimer's disease and kuru plaque amyloid in Creutzfeldt-Jakob disease. Brain Res 1991; 541: 163-6.
103. Sato W, Kadomatsu K, Yuzawa Y etal. Midkine is involved in neutrophil infiltration into the tubulointerstitium in ischemic renal injury. J Immunol 2001; 167: 3463-9.
104. Kosugi T, Yuzawa Y, Sato W etal. Growth factor midkine is involved in the pathogenesis of diabetic nephropathy. Am J Pathol 2006; 168: 9-19.
105. Kawai H, Sato W, Yuzawa Y etal. Lack of the growth factor midkine enhances survival against cisplatin-induced renal damage. Am J Pathol 2004; 165: 1603-12.
106. Horiba M, Kadomatsu K, Nakamura E etal. Neointima formation in a restenosis model is suppressed in midkine-deficient mice. J Clin Invest 2000; 105: 489-95.
107. Banno H, Takei Y, Muramatsu T, Komori K, Kadomatsu K. Controlled release of small interfering RNA targeting midkine attenuates intimal hyperplasia in vein grafts. J Vasc Surg 2006; 44: 633-41.
108. Narita H, Chen S, Komori K, Kadomatsu K. Midkine is expressed by infiltrating macrophages in in-stent restenosis in hypercholesterolemic rabbits. J Vasc Surg 2008; 47: 1322-9.
109. Wang J, Takeuchi H, Sonobe Y etal. Inhibition of midkine alleviates experimental autoimmune encephalomyelitis through the expansion of regulatory T cell population. Proc Natl Acad Sci U S A 2008; 105: 3915-20.
110. Horiba M, Kadomatsu K, Yasui K etal. Midkine plays a protective role against cardiac ischemia/reperfusion injury through a reduction of apoptotic reaction. Circulation 2006; 114: 1713-20.
111. Sumida A, Horiba M, Ishiguro H etal. Midkine gene transfer after myocardial infarction in rats prevents remodelling and ameliorates cardiac dysfunction. Cardiovasc Res 2010; 86: 113-21.
112. Ezquerra L, Herradon G, Nguyen T, Silos-Santiago I, Deuel TF. Midkine, a newly discovered regulator of the renin-angiotensin pathway in mouse aorta: Significance of the pleiotrophin/midkine developmental gene family in angiotensin II signaling. Biochem Biophys Res Commun 2005; 333: 636-43.
113. Hobo A, Yuzawa Y, Kosugi T etal. The growth factor midkine regulates the renin-angiotensin system in mice. J Clin Invest 2009; 119: 1616-25.
114. Kadomatsu K. Midkine regulation of the renin-angiotensin system. Curr Hypertens Rep 2010; 12: 74-9.
115. Kosugi T, Sato W. Midkine and the kidney: Health and diseases. Nephrol Dial Transplant 2012; 27: 16-21.
116. Callebaut C, Blanco J, Benkirane N etal. Identification of V3 loop-binding proteins as potential receptors implicated in the binding of HIV particles to CD4(+) cells. J Biol Chem 1998; 273: 21988-97.
117. Hovanessian AG, Puvion-Dutilleul F, Nisole S etal. The cell-surface-expressed nucleolin is associated with the actin cytoskeleton. Exp Cell Res 2000; 261: 312-28.
118. Take M, Tsutsui J, Obama H etal. Identification of nucleolin as a binding protein for midkine (MK) and heparin-binding growth associated molecule (HB-GAM). J Biochem (Tokyo) 1994; 116: 1063-8.
119. Said EA, Krust B, Nisole S, Svab J, Briand JP, Hovanessian AG. The anti-HIV cytokine midkine binds the cell surface-expressed nucleolin as a low affinity receptor. J Biol Chem 2002; 277: 37492-502.
120. Callebaut C, Nisole S, Briand JP, Krust B, Hovanessian AG. Inhibition of HIV infection by the cytokine midkine. Virology 2001; 281: 248-64.
121. Hovanessian AG. Midkine, a cytokine that inhibits HIV infection by binding to the cell surface expressed nucleolin. Cell Res 2006; 16: 174-81.