Transcriptomic Profile of Distal Middle Cerebral Artery from Moyamoya Disease Patients Reveals a Potential Unique Pathway

Authors

  • Yulius Hermanto Department of Neurosurgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan; 2Department of Neurosurgery, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia
  • Kent Doi Department of Neurosurgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan
  • Ahmad Faried Department of Neurosurgery, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia
  • Achmad Adam Department of Neurosurgery, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia
  • Tondi M. Tjili Neurosurgery Division, Department of Surgery, Faculty of Medicine, Riau University, Pekanbaru, Indonesia
  • Muhammad Z. Arifin Department of Neurosurgery, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia
  • Yasushi Takagi Department of Neurosurgery, Institute for Biological Sciences, Tokushima University, Tokushima, Japan
  • Susumu Miyamoto Department of Neurosurgery, Graduate School of Medicine, Kyoto University, Kyoto, Japan

DOI:

https://doi.org/10.3889/oamjms.2020.5513

Keywords:

Moyamoya disease, Microarray, Middle cerebral artery, RASopathies

Abstract

BACKGROUND: Moyamoya disease (MMD) is a peculiar disease, characterized by progressive steno-occlusion of the distal ends of bilateral internal carotid arteries and their proximal branches. Numerous studies of MMD investigated as a singular pathway, thus overlooked the complexity of MMD pathobiology.

AIM: In this study, we sought to investigate the gene expression in the involved arteries to reveal the novel mechanism of MMD.

MATERIALS AND METHODS: Eight middle cerebral artery (MCA) specimens were obtained from six patients underwent surgical procedure superficial temporal artery to MCA (STA-MCA bypass) for MMD and two control patients. We performed RNA extraction and microarray analysis with Agilent Whole Human Genome DNA microarray 4x44K ver.2.0 (Agilent Tech., Inc., Wilmington, DE, USA).

RESULTS: From 42,405 gene probes assayed, 921 gene probes were differentially regulated in MCA of patients with MMD. Subsequent pathway analysis with PANTHER database revealed that angiogenesis, inflammation, integrin, platelet-derived growth factor (PDGF), and WNT pathways were distinctly regulated in MMD. Among genes in aforementioned pathways, SOS1 and AKT2 were the mostly distinctly regulated genes and closely associated with RAS pathway.

CONCLUSION: The gene expression in MCA of patients with MMD was distinctly regulated in comparison with control MCA; presumably be useful for elucidating MMD pathobiology.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Plum Analytics Artifact Widget Block

References

Suzuki J, Takaku A. Cerebrovascular “moyamoya disease”: A disease showing abnormal net-like vessels in base of brain. Arch Neurol. 1969;20(3):288-99. https://doi.org/10.1001/archneur.1969.00480090076012 PMid:5775283 DOI: https://doi.org/10.1001/archneur.1969.00480090076012

Suzui H, Hoshimaru M, Takahashi JA, Kikuchi H, Fukumoto M, Ohta M, et al. Immunohistochemical reactions for fibroblast growth factor receptor in arteries of patients with moyamoya disease. Neurosurgery. 1994;35(1):20-5. https://doi.org/10.1097/00006123-199407000-00003 PMid:7936147 DOI: https://doi.org/10.1097/00006123-199407000-00003

Takagi Y, Hermanto Y, Takahashi JC, Funaki T, Kikuchi T, Mineharu Y, et al. Histopathological characteristics of distal middle cerebral artery in adult and pediatric patients with moyamoya disease. Neurol Med Chir (Tokyo). 2016;56:345-9. https://doi.org/10.2176/nmc.oa.2016-0031 PMid:27087193 DOI: https://doi.org/10.2176/nmc.oa.2016-0031

Liu W, Morito D, Takashima S, Mineharu Y, Kobayashi H, Hitomi T, et al. Identification of RNF213 as a susceptibility gene for moyamoya disease and its possible role in vascular development. PLoS One. 2011;6(7):e22542. https://doi.org/10.1371/journal.pone.0022542 PMid:21799892 DOI: https://doi.org/10.1371/journal.pone.0022542

Morimoto T, Mineharu Y, Kobayashi H, Harada KH, Funaki T, Takagi Y, et al. Significant association of the RNF213 p.R4810K poly-morphism with Quasi-moyamoya disease. J Stroke Cerebrovasc Dis. 2016;25(11):2632-6. https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.07.004 PMid:27476341 DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2016.07.004

Akagawa H, Mukawa M, Nariai T, Nomura S, Aihara Y, Onda H, et al. Novel and recurrent RNF213 variants in Japanese pediatric patients with moyamoya disease. Hum Genome Var. 2018;5:17060. https://doi.org/10.1038/hgv.2017.60 DOI: https://doi.org/10.1038/hgv.2017.60

Yamashita M, Oka K, Tanaka K. Histopathology of the brain vascular network in moyamoya disease. Stroke. 1983;14(1):50- 8. https://doi.org/10.1161/01.str.14.1.50 PMid:6823686 DOI: https://doi.org/10.1161/01.STR.14.1.50

Takebayashi S, Matsuo K, Kaneko M. Ultrastructural studies of cerebral arteries and collateral vessels in moyamoya disease. Stroke. 1984;15:728-32. https://doi.org/10.1161/01.str.15.4.728 DOI: https://doi.org/10.1161/01.STR.15.4.728

Takekawa Y, Umezawa T, Ueno Y, Sawada T, Kobayashi M. Pathological and immunohistochemical findings of an autopsy case of adult moyamoya disease. Neuropathol. 2004;24(3):236- 42. https://doi.org/10.1111/j.1440-1789.2004.00550.x PMid:15484702 DOI: https://doi.org/10.1111/j.1440-1789.2004.00550.x

Takagi Y, Kikuta K, Nozaki K, Hashimoto N. Histological features of middle cerebral arteries from patients treated for moyamoya disease. Neurol Med Chir (Tokyo). 2007;47(1):1-4. https://doi.org/10.2176/nmc.47.1 PMid:17245006 DOI: https://doi.org/10.2176/nmc.47.1

Takagi Y, Kikuta K, Sadamasa N, Nozaki K, Hashimoto N. Caspase-3-dependent apoptosis in middle cerebral arteries in patients with moyamoya disease. Neurosurgery. 2006;59(4):894- 900. https://doi.org/10.1227/01.neu.0000232771.80339.15 PMid:17038954 DOI: https://doi.org/10.1227/01.NEU.0000232771.80339.15

Aoyagi M, Fukai N, Sakamoto H, Shinkai T, Matsushima Y, Yamamoto M, et al. Altered cellular responses to serum mitogens, including platelet-derived growth factor, in cultured smooth muscle cells derived from arteries of patients with moyamoya disease. J Cell Physiol. 1991;147(2):191-8. https://doi.org/10.1002/jcp.1041470202 PMid:2040653 DOI: https://doi.org/10.1002/jcp.1041470202

Yoshimoto T, Houkin K, Takahashi A, Abe H. Angiogenic factors in moyamoya disease. Stroke. 1996;27:2160-5. https://doi.org/10.1161/01.str.27.12.2160 PMid:8969773 DOI: https://doi.org/10.1161/01.STR.27.12.2160

Hojo M, Hoshimaru M, Miyamoto S, Taki W, Nagata I, Asahi M, et al. Role of TGF-β1 in the pathogenesis of moyamoya disease. J Neurosurg. 1998;89(4):623-9. https://doi.org/10.3171/jns.1998.89.4.0623 PMid:9761057 DOI: https://doi.org/10.3171/jns.1998.89.4.0623

Nanba R, Kuroda S, Ishikawa T, Houkin K, Iwasaki Y. Increased expression of hepatocyte growth factor in cerebrospinal fluid and intracranial artery in moyamoya disease. Stroke. 2004;35(12):2837-42. https://doi.org/10.1161/01.str.0000148237.13659.e6 PMid:15528455 DOI: https://doi.org/10.1161/01.STR.0000148237.13659.e6

Kanoke A, Fujimura M, Niizuma K, Ito A, Sakata H, Sato-Maeda M, et al. Temporal profile of the vascular anatomy evaluated by 9.4- tesla magnetic resonance angiography and histological analysis in mice with R4859K mutation of RNF213, the susceptibility gene for moyamoya disease. Brain Res. 2015;1624:497-505. https://doi.org/10.1016/j.brainres.2015.07.039 PMid:26315378 DOI: https://doi.org/10.1016/j.brainres.2015.07.039

Kobayashi H, Matsuda Y, Hitomi T, Okuda H, Shioi H, Matsuda T, et al. Biochemical and functional characterization of RNF213 (Mysterin) R4810K, a susceptibility mutation of moyamoya disease, in angiongenesis in vitro and in vivo. J Am Heart Assoc. 2015;4(7):e002146. https://doi.org/10.1016/j.brainres.2015.07.039 PMid:26126547 DOI: https://doi.org/10.1161/JAHA.115.002146

Koss M, Scott RM, Irons MB, Smith ER, Ullrich NJ. Moyamoya syndrome associated with neurofibromatosis Type 1: Perioperative and long-term outcome after surgical revascularization. J Neurosurg Pediatr. 2013;11(4):417-25. https://doi.org/10.3171/2012.12.peds12281 PMid:23373626 DOI: https://doi.org/10.3171/2012.12.PEDS12281

Hyakuna N, Muramatsu H, Higa T, Chinen Y, Wang X, Kojima S. Germline mutation of CBL is associated with MMD in a child with juvenile myelomonocytic leukemia and noonan syndrome-like disorder. Pediatr Blood Cancer. 2015;62(3):542-44. https://doi.org/10.1002/pbc.25271 PMid:25283271 DOI: https://doi.org/10.1002/pbc.25271

Lo FS, Wang CJ, Wong MC, Lee NC. Moyamoya disease in two patients with Noonan-like syndrome with loose anagen hair. Am J Med Genet A. 2015;167(6):1285-8. https://doi.org/10.1002/ajmg.a.37053 PMid:25858597 DOI: https://doi.org/10.1002/ajmg.a.37053

See AP, Ropper AE, Underberg DL, Robertson RL, Scott RM, Smith ER. Down syndrome and moyamoya: Clinical presentation and surgical management. J Neursurg Pediatr. 2015;16(1):58- 63. https://doi.org/10.3171/2014.12.peds14563 PMid:25837890 DOI: https://doi.org/10.3171/2014.12.PEDS14563

Takagi Y, Kikuta KI, Nozaki K, Fujimoto M, Hayashi J, Imamura H, et al. Expression of hypoxia-inducing factor-1α and endoglin in intimal hyperplasia of the middle cerebral artery of patients with moyamoya disease. Neurosurgery. 2007;60(2):338-45; discussion 345. https://doi.org/10.1227/01.neu.0000249275.87310.ff PMid:17290185 DOI: https://doi.org/10.1227/01.NEU.0000249275.87310.FF

Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, et al. PANTHER: A library of protein families and sub-families indexed by function. Genome Res. 2003;13(9):2129-41. https://doi.org/10.1101/gr.772403 PMid:12952881 DOI: https://doi.org/10.1101/gr.772403

Suzuki J, Kodama N. Moyamoya disease a review. Stroke. 1989;14(1):104-9. PMid:6823678 DOI: https://doi.org/10.1161/01.STR.14.1.104

Miyawaki S, Imai H, Shimizu M, Yagi S, Ono H, Mukasa A, et al. Genetic variant RNF213 c.14576G>A in various phenotypes of intracranial major artery stenosis/occlusion. Stroke. 2013;44(10):2894-7. https://doi.org/10.1161/strokeaha.113.002477 PMid:23970789 DOI: https://doi.org/10.1161/STROKEAHA.113.002477

Hitomi T, Habu T, Kobayashi H, Okuda H, Harada KH, Osafune K, et al. Down- regulation of securin by the variant RNF213 R4810K (rs112735431, G>A) reduces angiogenic activity of induced pluripotent stem cell-derived vascular endothelial cells from moyamoya patients. Biochem Biophys Res Commun. 2013;438(1):13-9. https://doi.org/10.1016/j.bbrc.2013.07.004 PMid:23850618 DOI: https://doi.org/10.1016/j.bbrc.2013.07.004

Guo W, Giancotti FG. Integrin signaling during tumour progression. Nat Rev Mol Cell Biol. 2004;5(10):816-26. https://doi.org/10.1038/nrm1490 DOI: https://doi.org/10.1038/nrm1490

PMid:15459662

Liu A, Testa JR, Hamilton TC, Jove R, Nicosia SV, Cheng JQ. AKT2, a member of the protein kinase B family, is activated by growth factors, v-Ha-ras, and v-src through phosphatidylinositol 3-kinase in human ovarian epithelial cancer cells. Cancer Res. 1998;58(14):2973-7. PMid:9679957

Roberts AE, Araki T, Swanson KD, Montgomery KT, Schiripo TA, Joshi VA, et al. Germline gain-of-function mutations in SOS1 cause Noonan syndrome. Nat Genet. 2007:39(1):70-4. https://doi.org/10.1038/ng1926 PMid:17143285 DOI: https://doi.org/10.1038/ng1926

Tartaglia M, Kalidas K, Shaw A, Song X, Musat DL, van der Burgt, et al. PTPN11 mutations in Noonan syndrome: Molecular spectrum, genotype-phenotype correlation, and phenotypic heterogeneity. Am J Hum Genet. 2003;70:1555-63. https://doi.org/10.1086/340847 PMid:11992261 DOI: https://doi.org/10.1086/340847

Ganesan V, Kirkham FJ. Noonan syndrome and moyamoya. Pediatr Neurol. 1997;16(3):256-8. PMid:9165521 DOI: https://doi.org/10.1016/S0887-8994(97)89980-8

Schuster JM, Roberts TS. Symptomatic moyamoya disease and aortic coarctation in a patient with Noonan’s syndrome: Strategies for management. Pediatr Neurosurg. 1999;30(4):206-10. PMid:10420132 DOI: https://doi.org/10.1159/000028797

Tang KT, Yang W, Wong J, Lee KY. Noonan syndrome associated with moyamoya disease: Report of one case. Acta Pediatr Taiwan. 1999;40(4):274-6. PMid:10910629

Yamashita Y, Kusaga A, Koga Y, Nagamitsu S, Matsuishi T. Noonan syndrome, moyamoya-like vascular changes and antiphospholipid syndrome. Pediatr Neurol. 2004;31(5):364-6. https://doi.org/10.1016/j.pediatrneurol.2004.05.015 PMid:15519121 DOI: https://doi.org/10.1016/j.pediatrneurol.2004.05.015

Hung PC, Wang HS, Wong AM. Moyamoya syndrome in a child with Noonan syndrome. Pediatr Neurol. 2011;45(2):129-31. PMid:21763956 DOI: https://doi.org/10.1016/j.pediatrneurol.2011.03.007

Choi JH, Oh MY, Yum MS, Lee BH, Kim GH, Yoo HW. Moyamoya syndrome in a patient with Noonan-like syndrome with loose anagen hair. Pediatr Neurol. 2015;52(3):352-5. https://doi.org/10.1016/j.pediatrneurol.2014.11.017 PMid:25563136 DOI: https://doi.org/10.1016/j.pediatrneurol.2014.11.017

Hayashi K, Morofuji Y, Horie N, Izumo T. A case of neurofibromatosis type 1 complicated with repeated intracerebral hemorrhage due to quasi-moyamoya disease. J Stroke Cerebrovasc Dis. 2015;24(5):e109-13. https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.12.029 DOI: https://doi.org/10.1016/j.jstrokecerebrovasdis.2014.12.029

Ishiguro Y, Kubota T, Takenaka J, Maruyama K, Okumura A, Negoro T, et al. Cardio-facio-cutaneous syndrome and moyamoya syndrome. Brain Dev. 2002;24(4):245-9. https://doi.org/10.1016/s0387-7604(02)00014-1 PMid:12015168 DOI: https://doi.org/10.1016/S0387-7604(02)00014-1

Downloads

Published

2020-12-22

How to Cite

1.
Hermanto Y, Doi K, Faried A, Adam A, Tjili TM, Arifin MZ, Takagi Y, Miyamoto S. Transcriptomic Profile of Distal Middle Cerebral Artery from Moyamoya Disease Patients Reveals a Potential Unique Pathway. Open Access Maced J Med Sci [Internet]. 2020 Dec. 22 [cited 2024 Jun. 17];8(A):956-61. Available from: https://oamjms.eu/index.php/mjms/article/view/5513

Most read articles by the same author(s)

1 2 > >>