The heparin-binding growth factor midkine: the biological activities and candidate receptors

Journal of Biochemistry

Volumn 153, Issue 6, 2013, Pages 511-521

  Kadomatsu, Kenji ^a   Kishida, Satoshi ^a   Tsubota, Shoma ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

ALK; cancer; LRP1; midkine; PTP

Indexed keywords

ANAPLASTIC LYMPHOMA KINASE; CRIZOTINIB; GEMCITABINE; INTEGRIN; MIDKINE; NOTCH2 RECEPTOR; PROTEIN TYROSINE PHOSPHATASE EPSILON; PROTEOGLYCAN;

ALLERGIC ENCEPHALOMYELITIS; BIOLOGICAL ACTIVITY; BLADDER CARCINOMA; BLOOD PRESSURE; CANCER PROGNOSIS; CARCINOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CROHN DISEASE; GLIOMA; HUMAN; LUNG CANCER; MOLECULAR PATHOLOGY; MORPHOGENESIS; NEOINTIMA; NEUROBLASTOMA; NONHUMAN; PANCREAS ADENOCARCINOMA; PHENOTYPE; REVIEW; RHEUMATOID ARTHRITIS;

ALK; CANCER; LRP1; MIDKINE; PTPΖ;

ANIMALS; BINDING SITES; CARRIER PROTEINS; CYTOKINES; HEPARIN; HUMANS; INFLAMMATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASMS; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 5; SIGNAL TRANSDUCTION;

EID: 84878566210     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvt035     Document Type: Review

References (101)

1. Kadomatsu, K., Tomomura, M., and Muramatsu, T. (1988) 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. 151, 1312-1318
2. Tomomura, M., Kadomatsu, K., Matsubara, S., and Muramatsu, T. (1990) 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. 265, 10765-10770
3. Tomomura, M., Kadomatsu, K., Nakamoto, M., Muramatsu, H., Kondoh, H., Imagawa, K., and Muramatsu, T. (1990) A retinoic acid responsive gene, MK, produces a secreted protein with heparin binding activity. Biochem. Biophys. Res. Commun. 171, 603-609
4. Rauvala, H. (1989) An 18-kd heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J. 8, 2933-2941
5. Milner, P.G., Li, Y.S., Hoffman, R.M., Kodner, C.M., Siegel, N.R., and Deuel, T.F. (1989) A novel 17kD heparin-binding growth factor (HBGF-8) in bovine uterus: Purification and N-Terminal amino acid sequence. Biochem. Biophys. Res. Commun. 165, 1096-1103
6. Kadomatsu, K. and Muramatsu, T. (2004) Midkine and pleiotrophin in neural development and cancer. Cancer Lett. 204, 127-143
7. Muramatsu, T. (2010) Midkine, a heparin-binding cytokine with multiple roles in development, repair and diseases. Proc. Jpn Acad. Ser. B Phys. Biol. Sci. 86, 410-425
8. Sakamoto, K. and Kadomatsu, K. (2012) Midkine in the pathology of cancer, neural disease, and inflammation. Pathol. Int. 62, 445-455
9. Iwasaki, W., Nagata, K., Hatanaka, H., Inui, T., Kimura, T., Muramatsu, T., Yoshida, K., Tasumi, M., and Inagaki, F. (1997) Solution structure of midkine, a new heparin-binding growth factor. EMBO J. 16, 6936-6946
10. Kilpelainen, I., Kaksonen, M., Kinnunen, T., Avikainen, H., Fath, M., Linhardt, R.J., Raulo, E., and Rauvala, H. (2000) Heparin-binding growthassociated molecule contains two heparin-binding beta-sheet domains that are homologous to the thrombospondin type I repeat. J Biol. Chem. 275, 13564-13570
11. Tsutsui, J., Kadomatsu, K., Matsubara, S., Nakagawara, A., Hamanoue, M., Takao, S., Shimazu, H., Ohi, Y., and Muramatsu, T. (1993) A new family of heparin-binding growth/differentiation factors: Increased midkine expression in Wilms' tumor and other human carcinomas. Cancer Res. 53, 1281-1285
12. Wellstein, A., Fang, W.J., Khatri, A., Lu, Y., Swain, S.S., Dickson, R.B., Sasse, J., Riegel, A.T., and Lippman, M.E. (1992) A heparin-binding growth factor secreted from breast cancer cells homologous to a developmentally regulated cytokine. J. Biol. Chem. 267, 2582-2587
13. Akhter, S., Ichihara-Tanaka, K., Kojima, S., Muramatsu, H., Inui, T., Kimura, T., Kaneda, N., Talukder, A.H., Kadomatsu, K., Inagaki, F., and Muramatsu, T. (1998) Clusters of basic amino acids in midkine: Roles in neurite-promoting activity and plasminogen activator-enhancing activity. J. Biochem. 123, 1127-1136
14. Maeda, N., Ichihara-Tanaka, K., Kimura, T., Kadomatsu, K., Muramatsu, T., and Noda, M. (1999) 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. 274, 12474-12479
15. Wellstein, A. (2012) ALK receptor activation, ligands and therapeutic targeting in glioblastoma and in other cancers. Front. Oncol. 2, 192
16. Ikematsu, S., Yano, A., Aridome, K., Kikuchi, M., Kumai, H., Nagano, H., Okamoto, K., Oda, M., Sakuma, S., Aikou, T., Muramatsu, H., Kadomatsu, K., and Muramatsu, T. (2000) Serum midkine levels are increased in patients with various types of carcinomas. Br J. Cancer. 83, 701-706
17. Ikematsu, S., Nakagawara, A., Nakamura, Y., Ohira, M., Shinjo, M., Kishida, S., and Kadomatsu, K. (2008) Plasma midkine level is a prognostic factor for human neuroblastoma. Cancer Sci. 99, 2070-2074
18. Takei, Y., Kadomatsu, K., Matsuo, S., Itoh, H., Nakazawa, K., Kubota, S., and Muramatsu, T. (2001) Antisense oligodeoxynucleotide targeted to Midkine, a heparin-binding growth factor, suppresses tumorigenicity of mouse rectal carcinoma cells. Cancer Res. 61, 8486-8491
19. Kishida, S., Mu, P., Miyakawa, S., Fujiwara, M., Abe, T., Sakamoto, K., Onishi, A., Nakamura, Y., and Kadomatsu, K. (2013) Midkine Promotes Neuroblastoma through Notch2 Signaling. Cancer Res. 73, 1318-1327
20. Kang, H.C., Kim, I.J., Park, J.H., Shin, Y., Ku, J.L., Jung, M.S., Yoo, B.C., Kim, H.K., and Park, J.G. (2004) Identification of genes with differential expression in acquired drug-resistant gastric cancer cells using highdensity oligonucleotide microarrays. Clin. Cancer Res. 10, 272-284
21. Mirkin, B.L., Clark, S., Zheng, X., Chu, F., White, B.D., Greene, M., and Rebbaa, A. (2005) Identification of midkine as a mediator for intercellular transfer of drug resistance. Oncogene 24, 4965-4974
22. Takei, Y., Kadomatsu, K., Goto, T., and Muramatsu, T. (2006) Combinational antitumor effect of siRNA against midkine and paclitaxel on growth of human prostate cancer xenografts. Cancer 107, 864-873
23. Lorente, M., Torres, S., Salazar, M., Carracedo, A., Hernandez-Tiedra, S., Rodriguez-Fornes, F., Garcia-Taboada, E., Melendez, B., Mollejo, M., Campos-Martin, Y., Lakatosh, S.A., Barcia, J., Guzman, M., and Velasco, G. (2011) Stimulation of the midkine/ ALK axis renders glioma cells resistant to cannabinoid antitumoral action. Cell Death Differ. 18, 959-973
24. Horiba, M., Kadomatsu, K., Nakamura, E., Muramatsu, H., Ikematsu, S., Sakuma, S., Hayashi, K., Yuzawa, Y., Matsuo, S., Kuzuya, M., Kaname, T., Hirai, M., Saito, H., and Muramatsu, T. (2000) Neointima formation in a restenosis model is suppressed in midkine-deficient mice. J. Clin. Invest. 105, 489-495
25. Banno, H., Takei, Y., Muramatsu, T., Komori, K., and Kadomatsu, K. (2006) Controlled release of small interfering RNA targeting midkine attenuates intimal hyperplasia in vein grafts. J. Vasc. Surg. 44, 633-641
26. Sato, W., Kadomatsu, K., Yuzawa, Y., Muramatsu, H., Hotta, N., Matsuo, S., and Muramatsu, T. (2001) Midkine is involved in neutrophil infiltration into the tubulointerstitium in ischemic renal injury. J Immun. 167, 3463-3469
27. Sato, W., Takei, Y., Yuzawa, Y., Matsuo, S., Kadomatsu, K., and Muramatsu, T. (2005) Midkine antisense oligodeoxyribonucleotide inhibits renal damage induced by ischemic reperfusion. Kidney Int. 67, 1330-1339
28. Kawai, H., Sato, W., Yuzawa, Y., Kosugi, T., Matsuo, S., Takei, Y., Kadomatsu, K., and Muramatsu, T. (2004) Lack of the growth factor midkine enhances survival against cisplatin-induced renal damage. Am. J. Pathol. 165, 1603-1612
29. Kosugi, T., Yuzawa, Y., Sato, W., Arata-Kawai, H., Suzuki, N., Kato, N., Matsuo, S., and Kadomatsu, K. (2007) Midkine is involved in tubulointerstitial inflammation associated with diabetic nephropathy. Lab. Invest. 87, 903-913
30. Kosugi, T., Yuzawa, Y., Sato, W., Kawai, H., Matsuo, S., Takei, Y., Muramatsu, T., and Kadomatsu, K. (2006) Growth factor midkine is involved in the pathogenesis of diabetic nephropathy. Am. J. Pathol. 168, 9-19
31. Maruyama, K., Muramatsu, H., Ishiguro, N., and Muramatsu, T. (2004) Midkine, a heparin-binding growth factor, is fundamentally involved in the pathogenesis of rheumatoid arthritis. Arthritis Rheum. 50, 1420-1429
32. Krzystek-Korpacka, M., Neubauer, K., and Matusiewicz, M. (2010) Circulating midkine in Crohn's disease: Clinical implications. Inflamm. Bowel Dis. 16, 208-215
33. Wang, J., Takeuchi, H., Sonobe, Y., Jin, S., Mizuno, T., Miyakawa, S., Fujiwara, M., Nakamura, Y., Kato, T., Muramatsu, H., Muramatsu, T., and Suzumura, A. (2008) Inhibition of midkine alleviates experimental autoimmune encephalomyelitis through the expansion of regulatory T cell population. Proc. Natl. Acad. Sci. USA. 105, 3915-3920
34. Sonobe, Y., Li, H., Jin, S., Kishida, S., Kadomatsu, K., Takeuchi, H., Mizuno, T., and Suzumura, A. (2012) Midkine inhibits inducible regulatory T cell differentiation by suppressing the development of tolerogenic dendritic cells. J Immunol. 188, 2602-2611
35. Ezquerra, L., Herradon, G., Nguyen, T., Silos-Santiago, I., and Deuel, T.F. (2005) 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. 333, 636-643
36. Herradon, G., Ezquerra, L., Nguyen, T., Vogt, T.F., Bronson, R., Silos-Santiago, I., and Deuel, T.F. (2004) Pleiotrophin is an important regulator of the reninangiotensin system in mouse aorta. Biochem. Biophys. Res. Commun. 324, 1041-1047
37. Hobo, A., Yuzawa, Y., Kosugi, T., Kato, N., Asai, N., Sato, W., Maruyama, S., Ito, Y., Kobori, H., Ikematsu, S., Nishiyama, A., Matsuo, S., and Kadomatsu, K. (2009) The growth factor midkine regulates the reninangiotensin system in mice. J. Clin. Invest. 119, 1616-1625
38. Kadomatsu, K. (2010) Midkine regulation of the reninangiotensin system. Curr. Hypertens. Rep. 12, 74-79
39. Floege, J. and Uhlig, S. (2010) Kidney calling lung and call back: How organs talk to each other. Nephrol. Dial. Transplant. 25, 32-34
40. Toledano-Katchalski, H., Nir, R., Volohonsky, G., and Volk, T. (2007) Post-Transcriptional repression of the Drosophila midkine and pleiotrophin homolog miple by HOW is essential for correct mesoderm spreading. Development 134, 3473-3481
41. Winkler, C., Schafer, M., Duschl, J., Schartl, M., and Volff, J.N. (2003) Functional divergence of two zebrafish midkine growth factors following fish-specific gene duplication. Genome Res. 13, 1067-1081
42. Schafer, M., Rembold, M., Wittbrodt, J., Schartl, M., and Winkler, C. (2005) Medial floor plate formation in zebrafish consists of two phases and requires trunkderived Midkine-A. Genes Dev. 19, 897-902
43. Winkler, C. and Moon, R.T. (2001) Zebrafish mdk2, a novel secreted midkine, participates in posterior neurogenesis. Dev. Biol. 229, 102-118
44. Fan, Q.W., Muramatsu, T., and Kadomatsu, K. (2000) Distinct expression of midkine and pleiotrophin in the spinal cord and placental tissues during early mouse development. Dev. Growth Differ. 42, 113-119
45. Sekiguchi, K., Yokota, C., Asashima, M., Kaname, T., Fan, Q.W., Muramatsu, T., and Kadomatsu, K. (1995) Restricted expression of Xenopus midkine gene during early development. J. Biochem. 118, 94-100
46. Yokota, C., Takahashi, S., Eisaki, A., Asashima, M., Akhter, S., Muramatsu, T., and Kadomatsu, K. (1998) Midkine counteracts the activin signal in mesoderm induction and promotes neural formation. J. Biochem. 123, 339-346
47. Calinescu, A.A., Vihtelic, T.S., Hyde, D.R., and Hitchcock, P.F. (2009) Cellular expression of midkine-A and midkine-b during retinal development and photoreceptor regeneration in zebrafish. J. Comp. Neurol. 514, 1-10
48. Obama, H., Biro, S., Tashiro, T., Tsutsui, J., Ozawa, M., Yoshida, H., Tanaka, H., and Muramatsu, T. (1998) Myocardial infarction induces expression of midkine, a heparin-binding growth factor with reparative activity. Anticancer Res. 18, 145-152
49. Horiba, M., Kadomatsu, K., Yasui, K., Lee, J.K., Takenaka, H., Sumida, A., Kamiya, K., Chen, S., Sakuma, S., Muramatsu, T., and Kodama, I. (2006) Midkine plays a protective role against cardiac ischemia/ reperfusion injury through a reduction of apoptotic reaction. Circulation 114, 1713-1720
50. Takenaka, H., Horiba, M., Ishiguro, H., Sumida, A., Hojo, M., Usui, A., Akita, T., Sakuma, S., Ueda, Y., Kodama, I., and Kadomatsu, K. (2009) Midkine prevents ventricular remodeling and improves long-Term survival after myocardial infarction. Am J. Physiol. 296, H462-H469
51. Sumida, A., Horiba, M., Ishiguro, H., Takenaka, H., Ueda, N., Ooboshi, H., Opthof, T., Kadomatsu, K., and Kodama, I. (2010) Midkine gene transfer after myocardial infarction in rats prevents remodelling and ameliorates cardiac dysfunction. Cardiovasc. Res. 86, 113-121
52. Ishiguro, H., Horiba, M., Takenaka, H., Sumida, A., Opthof, T., Ishiguro, Y.S., Kadomatsu, K., Murohara, T., and Kodama, I. (2011) A single intracoronary injection of midkine reduces ischemia/reperfusion injury in Swine hearts: A novel therapeutic approach for acute coronary syndrome. Front. Physiol. 2, 27
53. Yoshida, Y., Goto, M., Tsutsui, J., Ozawa, M., Sato, E., Osame, M., and Muramatsu, T. (1995) Midkine is present in the early stage of cerebral infarct. Brain Res. Dev. Brain Res. 85, 25-30
54. Sakakima, H., Yoshida, Y., Muramatsu, T., Yone, K., Goto, M., Ijiri, K., and Izumo, S. (2004) Traumatic injury-induced midkine expression in the adult rat spinal cord during the early stage. J. Neurotrauma 21, 471-477
55. Yoshida, Y., Ikematsu, S., Moritoyo, T., Goto, M., Tsutsui, J., Sakuma, S., Osame, M., and Muramatsu, T. (2001) Intraventricular administration of the neurotrophic factor midkine ameliorates hippocampal delayed neuronal death following transient forebrain ischemia in gerbils. Brain Res. 894, 46-55
56. Masuda, K., Watanabe, I., Unoki, K., Ohba, N., and Muramatsu, T. (1995) Functional Rescue of photoreceptors from the damaging effects of constant light by survival-promoting factors in the rat. Invest. Ophthalmol. Vis. Sci. 36, 2142-2146
57. Unoki, K., Ohba, N., Arimura, H., Muramatsu, H., and Muramatsu, T. (1994) Rescue of photoreceptors rom the damaging effects of constant light by midkine, a retinoic acid-responsive gene product. Invest. Ophthalmol. Vis. Sci. 35, 4063-4068
58. Morris, S.W., Kirstein, M.N., Valentine, M.B., Dittmer, K., Shapiro, D.N., Look, A.T., and Saltman, D.L. (1995) Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non-Hodgkin's lymphoma. Science 267, 316-317
59. Shiota, M., Fujimoto, J., Semba, T., Satoh, H., Yamamoto, T., and Mori, S. (1994) Hyperphosphorylation of a novel 80 kDa protein-Tyrosine kinase similar to Ltk in a human Ki-1 lymphoma cell line, AMS3. Oncogene 9, 1567-1574
60. Soda, M., Choi, Y.L., Enomoto, M., Takada, S., Yamashita, Y., Ishikawa, S., Fujiwara, S., Watanabe, H., Kurashina, K., Hatanaka, H., Bando, M., Ohno, S., Ishikawa, Y., Aburatani, H., Niki, T., Sohara, Y., Sugiyama, Y., and Mano, H. (2007) Identification of the transforming EML4-ALK fusion gene in nonsmall-cell lung cancer. Nature 448, 561-566
61. Mano, H. (2012) ALKoma: A cancer subtype with a shared target. Cancer Discov. 2, 495-502
62. Stoica, G.E., Kuo, A., Aigner, A., Sunitha, I., Souttou, B., Malerczyk, C., Caughey, D.J., Wen, D., Karavanov, A., Riegel, A.T., and Wellstein, A. (2001) Identification of anaplastic lymphoma kinase as a receptor for the growth factor pleiotrophin. J. Biol. Chem. 276, 16772-16779
63. Stoica, G.E., Kuo, A., Powers, C., Bowden, E.T., Sale, E.B., Riegel, A.T., and Wellstein, A. (2002) Midkine binds to anaplastic lymphoma kinase (ALK) and acts as a growth factor for different cell types. J. Biol. Chem. 277, 35990-35998
64. Reiff, T., Huber, L., Kramer, M., Delattre, O., Janoueix-Lerosey, I., and Rohrer, H. (2011) Midkine and Alk signaling in sympathetic neuron proliferation and neuroblastoma predisposition. Development 138, 4699-4708
65. Mathivet, T., Mazot, P., and Vigny, M. (2007) In contrast to agonist monoclonal antibodies, both C-Terminal truncated form and full length form of Pleiotrophin failed to activate vertebrate ALK (anaplastic lymphoma kinase)? Cell. Signal. 19, 2434-2443
66. Lee, H.H., Norris, A., Weiss, J.B., and Frasch, M. (2003) Jelly belly protein activates the receptor tyrosine kinase Alk to specify visceral muscle pioneers. Nature 425, 507-512
67. Englund, C., Birve, A., Falileeva, L., Grabbe, C., and Palmer, R.H. (2006) Miple1 and miple2 encode a family of MK/PTN homologues in Drosophila melanogaster. Dev. Genes Evol. 216, 10-18
68. Maeda, N., Hamanaka, H., Shintani, T., Nishiwaki, T., and Noda, M. (1994) Multiple receptor-like protein tyrosine phosphatases in the form of chondroitin sulfate proteoglycan. FEBS Lett. 354, 67-70
69. Maeda, N. and Noda, M. (1998) Involvement of receptor-like protein tyrosine phosphatase zeta/RPTPbeta and its ligand pleiotrophin/heparin-binding growth-Associated molecule (HB-GAM) in neuronal migration. J. Cell Biol. 142, 203-216
70. Fukazawa, N., Yokoyama, S., Eiraku, M., Kengaku, M., and Maeda, N. (2008) Receptor type protein tyrosine phosphatase zeta-pleiotrophin signaling controls endocytic trafficking of DNER that regulates neuritogenesis. Mol. Cell. Biol. 28, 4494-4506
71. Qi, M., Ikematsu, S., Maeda, N., Ichihara-Tanaka, K., Sakuma, S., Noda, M., Muramatsu, T., and Kadomatsu, K. (2001) Haptotactic migration induced by midkine. Involvement of protein-Tyrosine phosphatase zeta. Mitogen-Activated protein kinase, and phosphatidylinositol 3-kinase. J. Biol. Chem. 276, 15868-15875
72. Cohen, S., Shoshana, O.Y., Zelman-Toister, E., Maharshak, N., Binsky-Ehrenreich, I., Gordin, M., Hazan-Halevy, I., Herishanu, Y., Shvidel, L., Haran, M., Leng, L., Bucala, R., Harroch, S., and Shachar, I. (2012) The cytokine midkine and its receptor RPTPzeta regulate B cell survival in a pathway induced by CD74. J. Immunol. 188, 259-269
73. Liedert, A., Mattausch, L., Rontgen, V., Blakytny, R., Vogele, D., Pahl, M., Bindl, R., Neunaber, C., Schinke, T., Harroch, S., Amling, M., and Ignatius, A. (2011) Midkine-deficiency increases the anabolic response of cortical bone to mechanical loading. Bone 48, 945-951
74. Muramatsu, H., Zou, P., Suzuki, H., Oda, Y., Chen, G.Y., Sakaguchi, N., Sakuma, S., Maeda, N., Noda, M., Takada, Y., and Muramatsu, T. (2004) alpha4beta1-And alpha6beta1-integrins are functional receptors for midkine, a heparin-binding growth factor. J. Cell Sci. 117, 5405-5415
75. Mikelis, C., Sfaelou, E., Koutsioumpa, M., Kieffer, N., and Papadimitriou, E. (2009) Integrin alpha(v)beta(3) is a pleiotrophin receptor required for pleiotrophin- induced endothelial cell migration through receptor protein tyrosine phosphatase beta/zeta. FASEB J. 23, 1459-1469
76. Perez-Pinera, P., Zhang, W., Chang, Y., Vega, J.A., and Deuel, T.F. (2007) Anaplastic lymphoma kinase is activated through the pleiotrophin/receptor protein-Tyrosine phosphatase beta/zeta signaling pathway: An alternative mechanism of receptor tyrosine kinase activation. J. Biol. Chem. 282, 28683-28690
77. Fujikawa, A., Fukada, M., Makioka, Y., Suzuki, R., Chow, J.P., Matsumoto, M., and Noda, M. (2011) Consensus substrate sequence for protein-Tyrosine phosphatase receptor type Z. J. Biol. Chem. 286, 37137-37146
78. Huang, Y., Hoque, M.O., Wu, F., Trink, B., Sidransky, D., and Ratovitski, E.A. (2008) Midkine induces epithelial-mesenchymal transition through Notch2/Jak2-Stat3 signaling in human keratinocytes. Cell Cycle 7, 1613-1622
79. Gungor, C., Zander, H., Effenberger, K.E., Vashist, Y.K., Kalinina, T., Izbicki, J.R., Yekebas, E., and Bockhorn, M. (2011) Notch signaling activated by replication stress-induced expression of midkine drives epithelial-mesenchymal transition and chemoresistance in pancreatic cancer. Cancer Res. 71, 5009-5019
80. Herz, J. and Strickland, D.K. (2001) LRP: A multifunctional scavenger and signaling receptor. J. Clin. Invest. 108, 779-784
81. Muramatsu, H., Zou, K., Sakaguchi, N., Ikematsu, S., Sakuma, S., and Muramatsu, T. (2000) LDL receptor-related protein as a component of the midkine receptor. Biochem. Biophys. Res. Commun. 270, 936-941
82. Shibata, Y., Muramatsu, T., Hirai, M., Inui, T., Kimura, T., Saito, H., McCormick, L.M., Bu, G., and Kadomatsu, K. (2002) Nuclear targeting by the growth factor midkine. Mol. Cell. Biol. 22, 6788-6796
83. Suzuki, N., Shibata, Y., Urano, T., Murohara, T., Muramatsu, T., and Kadomatsu, K. (2004) Proteasomal degradation of the nuclear targeting growth factor midkine. J. Biol. Chem. 279, 17785-17791
84. Lee, S.H., Suh, H.N., Lee, Y.J., Seo, B.N., Ha, J.W., and Han, H.J. (2012) Midkine prevented hypoxic injury of mouse embryonic stem cells through activation of Akt and HIF-1alpha via low-density lipoprotein receptor-related protein-1. J Cell. Physiol. 227, 1731-1739
85. Sakamoto, K., Bu, G., Chen, S., Takei, Y., Hibi, K., Kodera, Y., McCormick, L.M., Nakao, A., Noda, M., Muramatsu, T., and Kadomatsu, K. (2011) Premature ligand-receptor interaction during biosynthesis limits the production of growth factor midkine and its receptor LDL receptor-related protein 1. J. Biol. Chem. 286, 8405-8413
86. Fujisawa, K., Matsumoto, Y., Muramatsu, H., Shinzato, T., Hiramatsu, K., Horie, K., Cai, Z., Oka, H., Amano, I., Muramatsu, T., and Maeda, K. (1998) Increased serum midkine levels during hemodialysis using heparin in chronic renal failure. J. Biochem. 123, 864-869
87. Mitsiadis, T.A., Salmivirta, M., Muramatsu, T., Muramatsu, H., Rauvala, H., Lehtonen, E., Jalkanen, M., and Thesleff, I. (1995) Expression of the heparinbinding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 121, 37-51
88. Nakanishi, T., Kadomatsu, K., Okamoto, T., Ichihara-Tanaka, K., Kojima, T., Saito, H., Tomoda, Y., and Muramatsu, T. (1997) Expression of syndecan-1 and -3 during embryogenesis of the central nervous system in relation to binding with midkine. J. Biochem. 121, 197-205
89. Kojima, T., Katsumi, A., Yamazaki, T., Muramatsu, T., Nagasaka, T., Ohsumi, K., and Saito, H. (1996) Human ryudocan from endothelium-like cells binds basic fibroblast growth factor, midkine, and tissue factor pathway inhibitor. J. Biol. Chem. 271, 5914-5920
90. Muramatsu, H., Zou, P., Kurosawa, N., Ichihara-Tanaka, K., Maruyama, K., Inoh, K., Sakai, T., Chen, L., Sato, M., and Muramatsu, T. (2006) Female infertility in mice deficient in midkine and pleiotrophin, which form a distinct family of growth factors. Genes Cells 11, 1405-1417
91. Gramage, E., Putelli, A., Polanco, M.J., Gonzalez-Martin, C., Ezquerra, L., Alguacil, L.F., Perez-Pinera, P., Deuel, T.F., and Herradon, G. (2010) The neurotrophic factor pleiotrophin modulates amphetamineseeking behaviour and amphetamine-induced neurotoxic effects: Evidence from pleiotrophin knockout mice. Addict. Biol. 15, 403-412
92. Imai, S., Heino, T.J., Hienola, A., Kurata, K., Buki, K., Matsusue, Y., Vaananen, H.K., and Rauvala, H. (2009) Osteocyte-derived HB-GAM (pleiotrophin) is associated with bone formation and mechanical loading. Bone 44, 785-794
93. Neunaber, C., Catala-Lehnen, P., Beil, F.T., Marshall, R.P., Kanbach, V., Baranowsky, A., Lehmann, W., Streichert, T., Ignatius, A., Muramatsu, T., Schinke, T., and Amling, M. (2010) Increased trabecular bone formation in mice lacking the growth factor midkine. J. Bone Miner. Res. 25, 1724-1735
94. Nakamura, E., Kadomatsu, K., Yuasa, S., Muramatsu, H., Mamiya, T., Nabeshima, T., Fan, Q.W., Ishiguro, K., Igakura, T., Matsubara, S., Kaname, T., Horiba, M., Saito, H., and Muramatsu, T. (1998) 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 3, 811-822
95. Gramage, E., Martin, Y.B., Ramanah, P., Perez-Garcia, C., and Herradon, G. (2011) Midkine regulates amphetamine-induced astrocytosis in striatum but has no effects on amphetamine-induced striatal dopaminergic denervation and addictive effects: Functional differences between pleiotrophin and midkine. Neuroscience 190, 307-317
96. Bilsland, J.G., Wheeldon, A., Mead, A., Znamenskiy, P., Almond, S., Waters, K.A., Thakur, M., Beaumont, V., Bonnert, T.P., Heavens, R., Whiting, P., McAllister, G., and Munoz-Sanjuan, I. (2008) Behavioral and neurochemical alterations in mice deficient in anaplastic lymphoma kinase suggest therapeutic potential for psychiatric indications. Neuropsychopharmacology 33, 685-700
97. Harroch, S., Palmeri, M., Rosenbluth, J., Custer, A., Okigaki, M., Shrager, P., Blum, M., Buxbaum, J.D., and Schlessinger, J. (2000) No obvious abnormality in mice deficient in receptor protein tyrosine phosphatase beta. Mol. Cell. Biol. 20, 7706-7715
98. Huang, J.K., Ferrari, C.C., Monteiro de Castro, G., Lafont, D., Zhao, C., Zaratin, P., Pouly, S., Greco, B., and Franklin, R.J. (2012) Accelerated axonal loss following acute CNS demyelination in mice lacking protein tyrosine phosphatase receptor type Z. Am. J. Pathol. 181, 1518-1523
99. Hamada, Y., Kadokawa, Y., Okabe, M., Ikawa, M., Coleman, J.R., and Tsujimoto, Y. (1999) Mutation in ankyrin repeats of the mouse Notch2 gene induces early embryonic lethality. Development 126, 3415-3424
100. Herz, J., Clouthier, D.E., and Hammer, R.E. (1992) LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell 71, 411-421
101. Sheppard, D. (2000) In vivo functions of integrins: Lessons from null mutations in mice. Matrix Biol. 19, 203-209