nach oben

Brain Tumor Pathology

Erschienen in:

06.04.2022 | Review Article

Implications of immune cells in oncolytic herpes simplex virotherapy for glioma

verfasst von: Yoshihiro Otani, Ji Young Yoo, Toshihiko Shimizu, Kazuhiko Kurozumi, Isao Date, Balveen Kaur

Erschienen in: Brain Tumor Pathology | Ausgabe 2/2022

Einloggen, um Zugang zu erhalten

Abstract

Despite current progress in treatment, glioblastoma (GBM) remains a lethal primary malignant tumor of the central nervous system. Although immunotherapy has recently achieved remarkable survival effectiveness in multiple malignancies, none of the immune checkpoint inhibitors (ICIs) for GBM have shown anti-tumor efficacy in clinical trials. GBM has a characteristic immunosuppressive tumor microenvironment (TME) that results in the failure of ICIs. Oncolytic herpes simplex virotherapy (oHSV) is the most advanced United States Food and Drug Administration-approved virotherapy for advanced metastatic melanoma patients. Recently, another oHSV, Delytact^®, was granted conditional approval in Japan against GBM, highlighting it as a promising treatment. Since oncolytic virotherapy can recruit abundant immune cells and modify the immune TME, oncolytic virotherapy for immunologically cold GBM will be an attractive therapeutic option for GBM. However, as these immune cells have roles in both anti-tumor and anti-viral immunity, fine-tuning of the TME using oncolytic virotherapy will be important to maximize the therapeutic efficacy. In this review, we discuss the current knowledge of oHSV, with a focus on the role of immune cells as friend or foe in oncolytic virotherapy.

Ostrom QT, Cioffi G, Gittleman H et al (2019) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2012–2016. Neuro Oncol 21(Supplement 5):v1–v100PubMedPubMedCentralCrossRef

Louis DN, Perry A, Wesseling P et al (2021) The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol 23(8):1231–1251PubMedCrossRef

Otani Y, Ichikawa T, Kurozumi K et al (2019) Dynamic reorganization of microtubule and glioma invasion. Acta Med Okayama 73(4):285–297PubMed

Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352(10):987–996PubMedCrossRef

Stupp R, Taillibert S, Kanner A et al (2017) Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA 318(23):2306–2316PubMedPubMedCentralCrossRef

Reardon DA, Brandes AA, Omuro A et al (2020) Effect of nivolumab vs bevacizumab in patients with recurrent glioblastoma: the CheckMate 143 phase 3 randomized clinical trial. JAMA Oncol 6(7):1003–1010PubMedCrossRef

Friebel E, Kapolou K, Unger S et al (2020) Single-cell mapping of human brain cancer reveals tumor-specific instruction of tissue-invading leukocytes. Cell 181(7):1626-1642.e1620PubMedCrossRef

Goswami S, Walle T, Cornish AE et al (2020) Immune profiling of human tumors identifies CD73 as a combinatorial target in glioblastoma. Nat Med 26(1):39–46PubMedCrossRef

Hilf N, Kuttruff-Coqui S, Frenzel K et al (2019) Actively personalized vaccination trial for newly diagnosed glioblastoma. Nature 565(7738):240–245PubMedCrossRef

10.

Keskin DB, Anandappa AJ, Sun J et al (2019) Neoantigen vaccine generates intratumoral T cell responses in phase Ib glioblastoma trial. Nature 565(7738):234–239PubMedCrossRef

11.

Maggs L, Cattaneo G, Dal AE et al (2021) CAR T cell-based immunotherapy for the treatment of glioblastoma. Front Neurosci 15:662064PubMedPubMedCentralCrossRef

12.

Quattrocchi KB, Miller CH, Cush S et al (1999) Pilot study of local autologous tumor infiltrating lymphocytes for the treatment of recurrent malignant gliomas. J Neurooncol 45(2):141–157PubMedCrossRef

13.

Desjardins A, Gromeier M, Herndon JE 2nd et al (2018) Recurrent glioblastoma treated with recombinant poliovirus. N Engl J Med 379(2):150–161PubMedPubMedCentralCrossRef

14.

Fares J, Ahmed AU, Ulasov IV et al (2021) Neural stem cell delivery of an oncolytic adenovirus in newly diagnosed malignant glioma: a first-in-human, phase 1, dose-escalation trial. Lancet Oncol 22(8):1103–1114PubMedCrossRef

15.

Kurozumi K, Fujii K, Shimazu Y et al (2020) Study protocol of a phase I/IIa clinical trial of Ad-SGE-REIC for treatment of recurrent malignant glioma. Future Oncol 16(6):151–159PubMedCrossRef

16.

Kurozumi K, Koizumi S, Otani Y (2021) Gene therapy and viral therapy for malignant glioma. No Shinkei Geka 49(3):608–616PubMed

17.

Lang FF, Conrad C, Gomez-Manzano C et al (2018) Phase I study of DNX-2401 (Delta-24-RGD) oncolytic adenovirus: replication and immunotherapeutic effects in recurrent malignant glioma. J Clin Oncol 36(14):1419–1427PubMedPubMedCentralCrossRef

18.

Russell L, Swanner J, Jaime-Ramirez AC et al (2018) PTEN expression by an oncolytic herpesvirus directs T-cell mediated tumor clearance. Nat Commun 9(1):5006PubMedPubMedCentralCrossRef

19.

Martuza RL, Malick A, Markert JM et al (1991) Experimental therapy of human glioma by means of a genetically engineered virus mutant. Science 252(5007):854–856PubMedCrossRef

20.

Hong B, Sahu U, Mullarkey MP et al (2022) Replication and spread of oncolytic herpes simplex virus in solid tumors. Viruses 14(1):118PubMedPubMedCentralCrossRef

21.

Mineta T, Rabkin SD, Yazaki T et al (1995) Attenuated multi-mutated herpes simplex virus-1 for the treatment of malignant gliomas. Nat Med 1(9):938–943PubMedCrossRef

22.

Zhou G, Roizman B (2006) Construction and properties of a herpes simplex virus 1 designed to enter cells solely via the IL-13alpha2 receptor. Proc Natl Acad Sci USA 103(14):5508–5513PubMedPubMedCentralCrossRef

23.

Uchida H, Marzulli M, Nakano K et al (2013) Effective treatment of an orthotopic xenograft model of human glioblastoma using an EGFR-retargeted oncolytic herpes simplex virus. Mol Ther 21(3):561–569PubMedCrossRef

24.

Shibata T, Uchida H, Shiroyama T et al (2016) Development of an oncolytic HSV vector fully retargeted specifically to cellular EpCAM for virus entry and cell-to-cell spread. Gene Ther 23(6):479–488PubMedCrossRef

25.

He B, Gross M, Roizman B (1997) The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 94(3):843–848PubMedPubMedCentralCrossRef

26.

Farassati F, Yang AD, Lee PW (2001) Oncogenes in Ras signalling pathway dictate host-cell permissiveness to herpes simplex virus 1. Nat Cell Biol 3(8):745–750PubMedCrossRef

27.

MacLean AR, ul-Fareed M, Robertson L et al (1991) Herpes simplex virus type 1 deletion variants 1714 and 1716 pinpoint neurovirulence-related sequences in Glasgow strain 17+ between immediate early gene 1 and the “a” sequence. J Gen Virol 72(Pt 3):631–639PubMedCrossRef

28.

Dufour F, Sasseville AM, Chabaud S et al (2011) The ribonucleotide reductase R1 subunits of herpes simplex virus types 1 and 2 protect cells against TNFα- and FasL-induced apoptosis by interacting with caspase-8. Apoptosis 16(3):256–271PubMedCrossRef

29.

Todo T, Martuza RL, Rabkin SD et al (2001) Oncolytic herpes simplex virus vector with enhanced MHC class I presentation and tumor cell killing. Proc Natl Acad Sci USA 98(11):6396–6401PubMedPubMedCentralCrossRef

30.

Goldsmith K, Chen W, Johnson DC et al (1998) Infected cell protein (ICP)47 enhances herpes simplex virus neurovirulence by blocking the CD8+ T cell response. J Exp Med 187(3):341–348PubMedPubMedCentralCrossRef

31.

Peters C, Paget M, Tshilenge KT et al (2018) Restriction of replication of oncolytic herpes simplex virus with a deletion of γ34.5 in glioblastoma stem-like cells. J Virol 92(15)

32.

Kambara H, Okano H, Chiocca EA et al (2005) An oncolytic HSV-1 mutant expressing ICP34.5 under control of a nestin promoter increases survival of animals even when symptomatic from a brain tumor. Cancer Res 65(7):2832–2839PubMedCrossRef

33.

Hu JC, Coffin RS, Davis CJ et al (2006) A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res 12(22):6737–6747PubMedCrossRef

34.

Kaufman HL, Ruby CE, Hughes T et al (2014) Current status of granulocyte-macrophage colony-stimulating factor in the immunotherapy of melanoma. J Immunother Cancer 2:11PubMedPubMedCentralCrossRef

35.

Cheema TA, Wakimoto H, Fecci PE et al (2013) Multifaceted oncolytic virus therapy for glioblastoma in an immunocompetent cancer stem cell model. Proc Natl Acad Sci USA 110(29):12006–12011PubMedPubMedCentralCrossRef

36.

Bolyard C, Meisen WH, Banasavadi-Siddegowda Y et al (2017) BAI1 orchestrates macrophage inflammatory response to HSV infection—implications for oncolytic viral therapy. Clin Cancer Res 23(7):1809–1819PubMedCrossRef

37.

Fujii K, Kurozumi K, Ichikawa T et al (2013) The integrin inhibitor cilengitide enhances the anti-glioma efficacy of vasculostatin-expressing oncolytic virus. Cancer Gene Ther 20(8):437–444PubMedPubMedCentralCrossRef

38.

Hardcastle J, Kurozumi K, Dmitrieva N et al (2010) Enhanced antitumor efficacy of vasculostatin (Vstat120) expressing oncolytic HSV-1. Mol Ther 18(2):285–294PubMedCrossRef

39.

Nair M, Khosla M, Otani Y et al (2020) Enhancing antitumor efficacy of heavily vascularized tumors by RAMBO virus through decreased tumor endothelial cell activation. Cancers (Basel). 12(4):1040PubMedCentralCrossRef

40.

Tomita Y, Kurozumi K, Yoo JY et al (2019) Oncolytic herpes virus armed with vasculostatin in combination with bevacizumab abrogates glioma invasion via the CCN1 and AKT signaling pathways. Mol Cancer Ther 18(8):1418–1429PubMedCrossRef

41.

Brennan CW, Verhaak RG, McKenna A et al (2013) The somatic genomic landscape of glioblastoma. Cell 155(2):462–477PubMedPubMedCentralCrossRef

42.

Rutledge WC, Kong J, Gao J et al (2013) Tumor-infiltrating lymphocytes in glioblastoma are associated with specific genomic alterations and related to transcriptional class. Clin Cancer Res 19(18):4951–4960PubMedCrossRef

43.

Markert JM, Medlock MD, Rabkin SD et al (2000) Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial. Gene Ther 7(10):867–874PubMedCrossRef

44.

Markert JM, Razdan SN, Kuo HC et al (2014) A phase 1 trial of oncolytic HSV-1, G207, given in combination with radiation for recurrent GBM demonstrates safety and radiographic responses. Mol Ther 22(5):1048–1055PubMedPubMedCentralCrossRef

45.

Friedman GK, Johnston JM, Bag AK et al (2021) Oncolytic HSV-1 G207 immunovirotherapy for pediatric high-grade gliomas. N Engl J Med 384(17):1613–1622PubMedPubMedCentralCrossRef

46.

Waters AM, Johnston JM, Reddy AT et al (2017) Rationale and design of a phase 1 clinical trial to evaluate HSV G207 alone or with a single radiation dose in children with progressive or recurrent malignant supratentorial brain tumors. Hum Gene Ther Clin Dev 28(1):7–16PubMedPubMedCentralCrossRef

47.

Bernstock JD, Bag AK, Fiveash J et al (2020) Design and rationale for first-in-human phase 1 immunovirotherapy clinical trial of oncolytic HSV G207 to treat malignant pediatric cerebellar brain tumors. Hum Gene Ther 31(19–20):1132–1139PubMedPubMedCentralCrossRef

48.

Friedman GK, Bernstock JD, Chen D et al (2018) Enhanced sensitivity of patient-derived pediatric high-grade brain tumor xenografts to oncolytic HSV-1 virotherapy correlates with nectin-1 expression. Sci Rep 8(1):13930PubMedPubMedCentralCrossRef

49.

Rampling R, Cruickshank G, Papanastassiou V et al (2000) Toxicity evaluation of replication-competent herpes simplex virus (ICP 345 null mutant 1716) in patients with recurrent malignant glioma. Gene Ther 7(10):859–866PubMedCrossRef

50.

Papanastassiou V, Rampling R, Fraser M et al (2002) The potential for efficacy of the modified (ICP 34.5(-)) herpes simplex virus HSV1716 following intratumoural injection into human malignant glioma: a proof of principle study. Gene Ther 9(6):398–406PubMedCrossRef

51.

Harrow S, Papanastassiou V, Harland J et al (2004) HSV1716 injection into the brain adjacent to tumour following surgical resection of high-grade glioma: safety data and long-term survival. Gene Ther 11(22):1648–1658PubMedCrossRef

52.

Chiocca EA, Solomon I, Nakashima H et al (2021) First-in-human CAN-3110 (ICP-34.5 expressing HSV-1 oncolytic virus) in patients with recurrent high-grade glioma. J Clin Oncol 39(15_suppl):2009CrossRef

53.

Kurozumi K, Hardcastle J, Thakur R et al (2007) Effect of tumor microenvironment modulation on the efficacy of oncolytic virus therapy. J Natl Cancer Inst 99(23):1768–1781PubMedCrossRef

54.

Hong B, Muili K, Bolyard C et al (2019) Suppression of HMGB1 released in the glioblastoma tumor microenvironment reduces tumoral edema. Mol Ther Oncolytics 12:93–102PubMedCrossRef

55.

Saha D, Martuza RL, Rabkin SD (2017) Macrophage polarization contributes to glioblastoma eradication by combination immunovirotherapy and immune checkpoint blockade. Cancer Cell 32(2):253-267.e255PubMedPubMedCentralCrossRef

56.

Kim Y, Yoo JY, Lee TJ et al (2018) Complex role of NK cells in regulation of oncolytic virus-bortezomib therapy. Proc Natl Acad Sci USA 115(19):4927–4932PubMedPubMedCentralCrossRef

57.

Yoo JY, Jaime-Ramirez AC, Bolyard C et al (2016) Bortezomib treatment sensitizes oncolytic HSV-1-treated tumors to NK cell immunotherapy. Clin Cancer Res 22(21):5265–5276PubMedPubMedCentralCrossRef

58.

Otani Y, Yoo JY, Lewis CT et al (2022) NOTCH-induced MDSC recruitment after oHSV virotherapy in CNS cancer models modulates antitumor immunotherapy. Clin Cancer Res 28(7):1460–1473PubMedCrossRef

59.

Bernstock JD, Vicario N, Rong L et al (2019) A novel in situ multiplex immunofluorescence panel for the assessment of tumor immunopathology and response to virotherapy in pediatric glioblastoma reveals a role for checkpoint protein inhibition. Oncoimmunology 8(12):e1678921PubMedPubMedCentralCrossRef

60.

Kaufman HL, Kohlhapp FJ, Zloza A (2015) Oncolytic viruses: a new class of immunotherapy drugs. Nat Rev Drug Discov 14(9):642–662PubMedPubMedCentralCrossRef

61.

Serrano-Del Valle A, Anel A, Naval J et al (2019) Immunogenic cell death and immunotherapy of multiple myeloma. Front Cell Dev Biol 7:50PubMedPubMedCentralCrossRef

62.

Alvarez-Breckenridge CA, Yu J, Price R et al (2012) NK cells impede glioblastoma virotherapy through NKp30 and NKp46 natural cytotoxicity receptors. Nat Med 18(12):1827–1834PubMedPubMedCentralCrossRef

63.

Han J, Chen X, Chu J et al (2015) TGFβ treatment enhances glioblastoma virotherapy by inhibiting the innate immune response. Cancer Res 75(24):5273–5282PubMedPubMedCentralCrossRef

64.

Hambardzumyan D, Gutmann DH, Kettenmann H (2016) The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci 19(1):20–27PubMedPubMedCentralCrossRef

65.

Van Hove H, Martens L, Scheyltjens I et al (2019) A single-cell atlas of mouse brain macrophages reveals unique transcriptional identities shaped by ontogeny and tissue environment. Nat Neurosci 22(6):1021–1035PubMedCrossRef

66.

Wang Q, Hu B, Hu X et al (2017) Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment. Cancer Cell 32(1):42-56.e46PubMedPubMedCentralCrossRef

67.

Uneda A, Kurozumi K, Fujimura A et al (2021) Differentiated glioblastoma cells accelerate tumor progression by shaping the tumor microenvironment via CCN1-mediated macrophage infiltration. Acta Neuropathol Commun 9(1):29PubMedPubMedCentralCrossRef

68.

Denton NL, Chen CY, Scott TR et al (2016) Tumor-associated macrophages in oncolytic virotherapy: friend or foe? Biomedicines 4(3):13PubMedCentralCrossRef

69.

Meisen WH, Wohleb ES, Jaime-Ramirez AC et al (2015) The impact of macrophage- and microglia-secreted TNFalpha on oncolytic HSV-1 therapy in the glioblastoma tumor microenvironment. Clin Cancer Res 21(14):3274–3285PubMedPubMedCentralCrossRef

70.

Delwar ZM, Kuo Y, Wen YH et al (2018) Oncolytic virotherapy blockade by microglia and macrophages requires STAT1/3. Cancer Res 78(3):718–730PubMedCrossRef

71.

Fortin C, Yang Y, Huang X (2017) Monocytic myeloid-derived suppressor cells regulate T-cell responses against vaccinia virus. Eur J Immunol 47(6):1022–1031PubMedPubMedCentralCrossRef

72.

Tan Z, Liu L, Chiu MS et al (2019) Virotherapy-recruited PMN-MDSC infiltration of mesothelioma blocks antitumor CTL by IL-10-mediated dendritic cell suppression. Oncoimmunology. 8(1):e1518672PubMedCrossRef

73.

Clements DR, Sterea AM, Kim Y et al (2015) Newly recruited CD11b+, GR-1+, Ly6C(high) myeloid cells augment tumor-associated immunosuppression immediately following the therapeutic administration of oncolytic reovirus. J Immunol 194(9):4397–4412PubMedCrossRef

74.

Otani Y, Yoo JY, Chao S et al (2020) Oncolytic HSV-infected glioma cells activate NOTCH in adjacent tumor cells sensitizing tumors to gamma secretase inhibition. Clin Cancer Res 26(10):2381–2392PubMedPubMedCentralCrossRef

75.

Chang AL, Miska J, Wainwright DA et al (2016) CCL2 produced by the glioma microenvironment is essential for the recruitment of regulatory T cells and myeloid-derived suppressor cells. Cancer Res 76(19):5671–5682PubMedPubMedCentralCrossRef

76.

Alayo QA, Ito H, Passaro C et al (2020) Glioblastoma infiltration of both tumor- and virus-antigen specific cytotoxic T cells correlates with experimental virotherapy responses. Sci Rep 10(1):5095PubMedPubMedCentralCrossRef

77.

Ramelyte E, Tastanova A, Balázs Z et al (2021) Oncolytic virotherapy-mediated anti-tumor response: a single-cell perspective. Cancer Cell 39(3):394-406.e394PubMedCrossRef

78.

Markert JM, Liechty PG, Wang W et al (2009) Phase Ib trial of mutant herpes simplex virus G207 inoculated pre-and post-tumor resection for recurrent GBM. Mol Ther 17(1):199–207PubMedCrossRef

79.

Todo T (2019) ATIM-14. Results of phase ii clinical trial of oncolytic herpes virus G47δ in patients with glioblastomA. Neuro Oncol 21(Suppl 6):vi4PubMedCentralCrossRef

Titel: Implications of immune cells in oncolytic herpes simplex virotherapy for glioma
verfasst von: Yoshihiro Otani
Ji Young Yoo
Toshihiko Shimizu
Kazuhiko Kurozumi
Isao Date
Balveen Kaur
Publikationsdatum: 06.04.2022
Verlag: Springer Nature Singapore
Erschienen in: Brain Tumor Pathology / Ausgabe 2/2022
Print ISSN: 1433-7398
Elektronische ISSN: 1861-387X
DOI: https://doi.org/10.1007/s10014-022-00431-8

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Neu im Fachgebiet Neurologie

Schützt Olivenöl vor dem Tod durch Demenz?

10.05.2024 Morbus Alzheimer Nachrichten

Konsumieren Menschen täglich 7 Gramm Olivenöl, ist ihr Risiko, an einer Demenz zu sterben, um mehr als ein Viertel reduziert – und dies weitgehend unabhängig von ihrer sonstigen Ernährung. Dafür sprechen Auswertungen zweier großer US-Studien.

Bluttest erkennt Parkinson schon zehn Jahre vor der Diagnose

10.05.2024 Parkinson-Krankheit Nachrichten

Ein Bluttest kann abnorm aggregiertes Alpha-Synuclein bei einigen Menschen schon zehn Jahre vor Beginn der motorischen Parkinsonsymptome nachweisen. Mit einem solchen Test lassen sich möglicherweise Prodromalstadien erfassen und die Betroffenen früher behandeln.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Wartezeit nicht kürzer, aber Arbeit flexibler

Psychotherapie Medizin aktuell

Fünf Jahren nach der Neugestaltung der Psychotherapie-Richtlinie wurden jetzt die Effekte der vorgenommenen Änderungen ausgewertet. Das Hauptziel der Novellierung war eine kürzere Wartezeit auf Therapieplätze. Dieses Ziel wurde nicht erreicht, es gab jedoch positive Auswirkungen auf andere Bereiche.

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 2/2022

A patient with two gliomas with independent oligodendroglioma and glioblastoma biology proved by DNA-methylation profiling: a case report and review of the literature

Preface for Brain Tumor Pathology vol. 39 issue 2

Histopathological predictors of progression-free survival in atypical meningioma: a single-center retrospective cohort and meta-analysis

The 2021 WHO classification of tumors, 5th edition, central nervous system tumors: the 10 basic principles

The oligodendroglial histological features are not independently predictive of patient prognosis in lower-grade gliomas