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Article ; Online: Balancing safety and efficacy: tuning the biodistribution and pharmacokinetics of cytokine immunotherapies.

Momin, Noor

2023 Volume 84, Page(s) 102994

Abstract: Modulating the immune system shows promise in treating various conditions such as autoimmune, malignant, inflammatory, and infectious diseases. While immunotherapies can provide significant clinical benefits, they can also trigger debilitating immune- ... ...

Abstract	Modulating the immune system shows promise in treating various conditions such as autoimmune, malignant, inflammatory, and infectious diseases. While immunotherapies can provide significant clinical benefits, they can also trigger debilitating immune-related toxicities. Achieving a balance between safety and efficacy of immunotherapy remains a significant engineering challenge. A complex immune response can be simplified into a sequence of coordinated signals with precise spatial and temporal arrangements. Mimicking or inhibiting these signals with protein immunotherapies relies on engineering them with specific biodistribution and pharmacokinetic properties. This review summarizes principles governing the movement of therapeutic proteins (i.e. biologics), focusing on cytokine immunotherapies injected intravenously or locally, and highlights approaches and considerations to balance their efficacy and safety.
MeSH term(s)	Humans ; Tissue Distribution ; Cytokines ; Immunotherapy ; Neoplasms/therapy
Chemical Substances	Cytokines
Language	English
Publishing date	2023-10-06
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	1052045-4
ISSN	1879-0429 ; 0958-1669
ISSN (online)	1879-0429
ISSN	0958-1669
DOI	10.1016/j.copbio.2023.102994
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Article: Tumor-localized interleukin-2 and interleukin-12 combine with radiation therapy to safely potentiate regression of advanced malignant melanoma in pet dogs.

Stinson, Jordan A / Barbosa, Matheus Moreno P / Sheen, Allison / Momin, Noor / Fink, Elizabeth / Hampel, Jordan / Selting, Kimberly / Kamerer, Rebecca / Bailey, Keith L / Wittrup, K Dane / Fan, Timothy M

bioRxiv : the preprint server for biology

2024

Abstract: The clinical use of interleukin-2 and -12 cytokines against cancer is limited by their narrow therapeutic windows due to on-target, off-tumor activation of immune cells when delivered systemically. Engineering IL-2 and IL-12 to bind to extracellular ... ...

Abstract	The clinical use of interleukin-2 and -12 cytokines against cancer is limited by their narrow therapeutic windows due to on-target, off-tumor activation of immune cells when delivered systemically. Engineering IL-2 and IL-12 to bind to extracellular matrix collagen allows these cytokines to be retained within tumors after intralesional injection, overcoming these clinical safety challenges. While this approach has potentiated responses in syngeneic mouse tumors without toxicity, the complex tumor-immune interactions in human cancers are difficult to recapitulate in mouse models of cancer. This has driven an increased role for comparative oncology clinical trials in companion (pet) dogs with spontaneous cancers that feature analogous tumor and immune biology to human cancers. Here, we report the results from a dose-escalation clinical trial of intratumoral collagen-binding IL-2 and IL-12 cytokines in pet dogs with malignant melanoma, observing encouraging local and regional responses to therapy that may suggest human clinical benefit with this approach.
Language	English
Publishing date	2024-02-14
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.02.12.579965
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Article ; Online: Intratumoral nanobody-IL-2 fusions that bind the tumor extracellular matrix suppress solid tumor growth in mice.

Lutz, Emi A / Jailkhani, Noor / Momin, Noor / Huang, Ying / Sheen, Allison / Kang, Byong H / Wittrup, K Dane / Hynes, Richard O

PNAS nexus

2022 Volume 1, Issue 5, Page(s) pgac244

Abstract: Confining cytokine exposure to the tumors would greatly enhance cancer immunotherapy safety and efficacy. Immunocytokines, cytokines fused to tumor-targeting antibodies, have been developed with this intention, but without significant clinical success to ...

Abstract	Confining cytokine exposure to the tumors would greatly enhance cancer immunotherapy safety and efficacy. Immunocytokines, cytokines fused to tumor-targeting antibodies, have been developed with this intention, but without significant clinical success to date. A critical limitation is uptake by receptor-expressing cells in the blood, that decreases the dose at the tumor and engenders toxicity. Small-format immunocytokines, constructed with antibody fragments, are hypothesized to improve tumor specificity due to rapid systemic clearance. However, effective design criteria for small-format immunocytokines need further examination. Here, we engineer small interleukin-2 (IL-2) immunocytokines fused to nanobodies with nanomolar to picomolar affinities for the tumor-specific EIIIB domain of fibronectin (also known as EDB). Upon intravenous delivery into immunocompetent mice, such immunocytokines led to similar tumor growth delay as size-matched untargeted IL-2. Intratumoral (i.t.) delivery imparted improved survival dependent on affinity to EIIIB. I.t. administration offers a promising avenue to deliver small-format immunocytokines, given effective affinity for the tumor microenvironment.
Language	English
Publishing date	2022-11-03
Publishing country	England
Document type	Journal Article
ISSN	2752-6542
ISSN (online)	2752-6542
DOI	10.1093/pnasnexus/pgac244
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Article ; Online: Ultrasonographic assessment of pulmonary and Central venous congestion in experimental heart failure.

Hegemann, Niklas / Sang, Pengchao / Kim, Jonathan H / Koçana, Ceren / Momin, Noor / Klages, Jan / Kucherenko, Mariya M / Knosalla, Christoph / O'Brien, Benjamin / Simmons, Szandor / Nahrendorf, Matthias / Kuebler, Wolfgang M / Grune, Jana

American journal of physiology. Heart and circulatory physiology

2023 Volume 326, Issue 2, Page(s) H433–H440

Abstract: Pulmonary and systemic congestion as a consequence of heart failure are clinically recognized as alarm signals for clinical outcome and mortality. Although signs and symptoms of congestion are well detectable in patients, monitoring of congestion in ... ...

Abstract	Pulmonary and systemic congestion as a consequence of heart failure are clinically recognized as alarm signals for clinical outcome and mortality. Although signs and symptoms of congestion are well detectable in patients, monitoring of congestion in small animals with heart failure lacks adequate noninvasive methodology yet. Here, we developed a novel ultrasonography-based scoring system to assess pulmonary and systemic congestion in experimental heart failure, by using lung ultrasound (LUS) and imaging of the inferior vena cava (Cava), termed CavaLUS. CavaLUS was established and tested in a rat model of supracoronary aortic banding and a mouse model of myocardial infarction, providing high sensitivity and specificity while correlating to numerous parameters of cardiac performance and disease severity. CavaLUS, therefore, provides a novel comprehensive tool for experimental heart failure in small animals to noninvasively assess congestion.
MeSH term(s)	Humans ; Mice ; Animals ; Rats ; Hyperemia/diagnostic imaging ; Lung/diagnostic imaging ; Ultrasonography/methods ; Heart Failure/diagnostic imaging ; Heart Failure/etiology ; Vena Cava, Inferior/diagnostic imaging
Language	English
Publishing date	2023-12-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	603838-4
ISSN	1522-1539 ; 0363-6135
ISSN (online)	1522-1539
ISSN	0363-6135
DOI	10.1152/ajpheart.00735.2023
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Article ; Online: Overcoming lung cancer immunotherapy resistance by combining nontoxic variants of IL-12 and IL-2.

Horton, Brendan L / D'Souza, Alicia D / Zagorulya, Maria / McCreery, Chloe V / Abhiraman, Gita C / Picton, Lora / Sheen, Allison / Agarwal, Yash / Momin, Noor / Wittrup, K Dane / White, Forest M / Garcia, K Christopher / Spranger, Stefani

JCI insight

2023 Volume 8, Issue 19

Abstract: Engineered cytokine-based approaches for immunotherapy of cancer are poised to enter the clinic, with IL-12 being at the forefront. However, little is known about potential mechanisms of resistance to cytokine therapies. We found that orthotopic murine ... ...

Abstract	Engineered cytokine-based approaches for immunotherapy of cancer are poised to enter the clinic, with IL-12 being at the forefront. However, little is known about potential mechanisms of resistance to cytokine therapies. We found that orthotopic murine lung tumors were resistant to systemically delivered IL-12 fused to murine serum albumin (MSA, IL12-MSA) because of low IL-12 receptor (IL-12R) expression on tumor-reactive CD8+ T cells. IL2-MSA increased binding of IL12-MSA by tumor-reactive CD8+ T cells, and combined administration of IL12-MSA and IL2-MSA led to enhanced tumor-reactive CD8+ T cell effector differentiation, decreased numbers of tumor-infiltrating CD4+ regulatory T cells, and increased survival of lung tumor-bearing mice. Predictably, the combination of IL-2 and IL-12 at therapeutic doses led to significant dose-limiting toxicity. Administering IL-12 and IL-2 analogs with preferential binding to cells expressing Il12rb1 and CD25, respectively, led to a significant extension of survival in mice with lung tumors while abrogating dose-limiting toxicity. These findings suggest that IL-12 and IL-2 represent a rational approach to combination cytokine therapy whose dose-limiting toxicity can be overcome with engineered cytokine variants.
MeSH term(s)	Mice ; Animals ; Interleukin-12/genetics ; Interleukin-2/genetics ; Immunotherapy ; Cytokines ; Lung Neoplasms/genetics ; Lung Neoplasms/therapy
Chemical Substances	Interleukin-12 (187348-17-0) ; Interleukin-2 ; Cytokines
Language	English
Publishing date	2023-10-09
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2379-3708
ISSN (online)	2379-3708
DOI	10.1172/jci.insight.172728
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Article ; Online: Tissue-specific abundance of interferon-gamma drives regulatory T cells to restrain DC1-mediated priming of cytotoxic T cells against lung cancer.

Zagorulya, Maria / Yim, Leon / Morgan, Duncan M / Edwards, Austin / Torres-Mejia, Elen / Momin, Noor / McCreery, Chloe V / Zamora, Izabella L / Horton, Brendan L / Fox, James G / Wittrup, K Dane / Love, J Christopher / Spranger, Stefani

Immunity

2023 Volume 56, Issue 2, Page(s) 386–405.e10

Abstract: Local environmental factors influence ... ...

Abstract	Local environmental factors influence CD8
MeSH term(s)	Humans ; CD8-Positive T-Lymphocytes ; Interferon-gamma ; Lung Neoplasms ; T-Lymphocytes, Cytotoxic ; T-Lymphocytes, Regulatory
Chemical Substances	Interferon-gamma (82115-62-6) ; IFNG protein, human
Language	English
Publishing date	2023-02-02
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1217235-2
ISSN	1097-4180 ; 1074-7613
ISSN (online)	1097-4180
ISSN	1074-7613
DOI	10.1016/j.immuni.2023.01.010
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Zs.A 4227: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (2.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Collagen-Anchored Interleukin-2 and Interleukin-12 Safely Reprogram the Tumor Microenvironment in Canine Soft-Tissue Sarcomas.

Stinson, Jordan A / Sheen, Allison / Momin, Noor / Hampel, Jordan / Bernstein, Rebecca / Kamerer, Rebecca / Fadl-Alla, Bahaa / Samuelson, Jonathan / Fink, Elizabeth / Fan, Timothy M / Wittrup, K Dane

Clinical cancer research : an official journal of the American Association for Cancer Research

2023 Volume 29, Issue 11, Page(s) 2110–2122

Abstract: Purpose: Cytokine therapies such as IL2 and IL12 suffer from impractically small therapeutic windows driven by their on-target, off-tumor activity, limiting their clinical potential despite potent antitumor effects. We previously engineered cytokines ... ...

Abstract	Purpose: Cytokine therapies such as IL2 and IL12 suffer from impractically small therapeutic windows driven by their on-target, off-tumor activity, limiting their clinical potential despite potent antitumor effects. We previously engineered cytokines that bind and anchor to tumor collagen following intratumoral injection, and sought to test their safety and biomarker activity in spontaneous canine soft-tissue sarcomas (STS). Experimental design: Collagen-binding cytokines were canine-ized to minimize immunogenicity and were used in a rapid dose-escalation study in healthy beagles to identify a maximum tolerated dose. Ten client-owned pet dogs with STS were then enrolled into trial, receiving cytokines at different intervals prior to surgical tumor excision. Tumor tissue was analyzed through IHC and NanoString RNA profiling for dynamic changes within treated tumors. Archived, untreated STS samples were analyzed in parallel as controls. Results: Intratumorally administered collagen-binding IL2 and IL12 were well tolerated by STS-bearing dogs, with only Grade 1/2 adverse events observed (mild fever, thrombocytopenia, neutropenia). IHC revealed enhanced T-cell infiltrates, corroborated by an enhancement in gene expression associated with cytotoxic immune function. We found concordant increases in expression of counter-regulatory genes that we hypothesize would contribute to a transient antitumor effect, and confirmed in mouse models that combination therapy to inhibit this counter-regulation can improve responses to cytokine therapy. Conclusions: These results support the safety and activity of intratumorally delivered, collagen-anchoring cytokines for inflammatory polarization of the canine STS tumor microenvironment. We are further evaluating the efficacy of this approach in additional canine cancers, including oral malignant melanoma.
MeSH term(s)	Mice ; Animals ; Dogs ; Interleukin-12/genetics ; Interleukin-2 ; Tumor Microenvironment ; Cytokines ; Melanoma ; Sarcoma/drug therapy ; Collagen
Chemical Substances	Interleukin-12 (187348-17-0) ; Interleukin-2 ; Cytokines ; Collagen (9007-34-5)
Language	English
Publishing date	2023-03-31
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1225457-5
ISSN	1557-3265 ; 1078-0432
ISSN (online)	1557-3265
ISSN	1078-0432
DOI	10.1158/1078-0432.CCR-23-0006
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Zs.A 4223: Show issues

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Article ; Online: Immunotherapy-induced antibodies to endogenous retroviral envelope glycoprotein confer tumor protection in mice.

Kang, Byong H / Momin, Noor / Moynihan, Kelly D / Silva, Murillo / Li, Yingzhong / Irvine, Darrell J / Wittrup, K Dane

PloS one

2021 Volume 16, Issue 4, Page(s) e0248903

Abstract: Following curative immunotherapy of B16F10 tumors, ~60% of mice develop a strong antibody response against cell-surface tumor antigens. Their antisera confer prophylactic protection against intravenous challenge with B16F10 cells, and also cross-react ... ...

Abstract	Following curative immunotherapy of B16F10 tumors, ~60% of mice develop a strong antibody response against cell-surface tumor antigens. Their antisera confer prophylactic protection against intravenous challenge with B16F10 cells, and also cross-react with syngeneic and allogeneic tumor cell lines MC38, EL.4, 4T1, and CT26. We identified the envelope glycoprotein (env) of a murine endogenous retrovirus (ERV) as the antigen accounting for the majority of this humoral response. A systemically administered anti-env monoclonal antibody cloned from such a response protects against tumor challenge, and prophylactic vaccination against the env protein protects a majority of naive mice from tumor establishment following subcutaneous inoculation with B16F10 cells. These results suggest the potential for effective prophylactic vaccination against analogous HERV-K env expressed in numerous human cancers.
MeSH term(s)	Animals ; Antibodies, Neoplasm/immunology ; Cell Line, Tumor ; Endogenous Retroviruses/immunology ; Gene Products, env/immunology ; Immunotherapy/methods ; Mice ; Mice, Inbred C57BL ; Neoplasms/immunology ; Neoplasms/therapy
Chemical Substances	Antibodies, Neoplasm ; Gene Products, env
Language	English
Publishing date	2021-04-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2267670-3
ISSN	1932-6203 ; 1932-6203
ISSN (online)	1932-6203
ISSN	1932-6203
DOI	10.1371/journal.pone.0248903
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Article ; Online: Alum-anchored intratumoral retention improves the tolerability and antitumor efficacy of type I interferon therapies.

Lutz, Emi A / Agarwal, Yash / Momin, Noor / Cowles, Sarah C / Palmeri, Joseph R / Duong, Ellen / Hornet, Vladlena / Sheen, Allison / Lax, Brianna M / Rothschilds, Adrienne M / Irvine, Darrell J / Spranger, Stefani / Wittrup, K Dane

Proceedings of the National Academy of Sciences of the United States of America

2022 Volume 119, Issue 36, Page(s) e2205983119

Abstract: Effective antitumor immunity in mice requires activation of the type I interferon (IFN) response pathway. IFNα and IFNβ therapies have proven promising in humans, but suffer from limited efficacy and high toxicity. Intratumoral IFN retention ameliorates ... ...

Abstract	Effective antitumor immunity in mice requires activation of the type I interferon (IFN) response pathway. IFNα and IFNβ therapies have proven promising in humans, but suffer from limited efficacy and high toxicity. Intratumoral IFN retention ameliorates systemic toxicity, but given the complexity of IFN signaling, it was unclear whether long-term intratumoral retention of type I IFNs would promote or inhibit antitumor responses. To this end, we compared the efficacy of IFNα and IFNβ that exhibit either brief or sustained retention after intratumoral injection in syngeneic mouse tumor models. Significant enhancement in tumor retention, mediated by anchoring these IFNs to coinjected aluminum-hydroxide (alum) particles, greatly improved both their tolerability and efficacy. The improved efficacy of alum-anchored IFNs could be attributed to sustained pleiotropic effects on tumor cells, immune cells, and nonhematopoietic cells. Alum-anchored IFNs achieved high cure rates of B16F10 tumors upon combination with either anti-PD-1 antibody or interleukin-2. Interestingly however, these alternative combination immunotherapies yielded disparate T cell phenotypes and differential resistance to tumor rechallenge, highlighting important distinctions in adaptive memory formation for combinations of type I IFNs with other immunotherapies.
MeSH term(s)	Alum Compounds/chemistry ; Aluminum Hydroxide/chemistry ; Animals ; Antineoplastic Agents/therapeutic use ; Disease Models, Animal ; Humans ; Immunotherapy/methods ; Immunotherapy/standards ; Interferon Type I/chemistry ; Interferon Type I/therapeutic use ; Interferon-alpha ; Interferon-beta ; Metal Nanoparticles/chemistry ; Metal Nanoparticles/therapeutic use ; Mice
Chemical Substances	Alum Compounds ; Antineoplastic Agents ; Interferon Type I ; Interferon-alpha ; Aluminum Hydroxide (5QB0T2IUN0) ; Interferon-beta (77238-31-4)
Language	English
Publishing date	2022-08-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2205983119
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Article ; Online: Maximizing response to intratumoral immunotherapy in mice by tuning local retention.

Momin, Noor / Palmeri, Joseph R / Lutz, Emi A / Jailkhani, Noor / Mak, Howard / Tabet, Anthony / Chinn, Magnolia M / Kang, Byong H / Spanoudaki, Virginia / Hynes, Richard O / Wittrup, K Dane

Nature communications

2022 Volume 13, Issue 1, Page(s) 109

Abstract: Direct injection of therapies into tumors has emerged as an administration route capable of achieving high local drug exposure and strong anti-tumor response. A diverse array of immune agonists ranging in size and target are under development as local ... ...

Abstract	Direct injection of therapies into tumors has emerged as an administration route capable of achieving high local drug exposure and strong anti-tumor response. A diverse array of immune agonists ranging in size and target are under development as local immunotherapies. However, due to the relatively recent adoption of intratumoral administration, the pharmacokinetics of locally-injected biologics remains poorly defined, limiting rational design of tumor-localized immunotherapies. Here we define a pharmacokinetic framework for biologics injected intratumorally that can predict tumor exposure and effectiveness. We find empirically and computationally that extending the tumor exposure of locally-injected interleukin-2 by increasing molecular size and/or improving matrix-targeting affinity improves therapeutic efficacy in mice. By tracking the distribution of intratumorally-injected proteins using positron emission tomography, we observe size-dependent enhancement in tumor exposure occurs by slowing the rate of diffusive escape from the tumor and by increasing partitioning to an apparent viscous region of the tumor. In elucidating how molecular weight and matrix binding interplay to determine tumor exposure, our model can aid in the design of intratumoral therapies to exert maximal therapeutic effect.
MeSH term(s)	Allografts ; Animals ; Carrier Proteins/genetics ; Carrier Proteins/immunology ; Cell Line, Tumor ; Collagen/genetics ; Collagen/immunology ; Female ; Gene Library ; Immunotherapy/methods ; Injections, Intralesional ; Interleukin-2/genetics ; Interleukin-2/immunology ; Interleukin-2/pharmacokinetics ; Interleukin-2/pharmacology ; Melanoma, Experimental/diagnostic imaging ; Melanoma, Experimental/genetics ; Melanoma, Experimental/mortality ; Melanoma, Experimental/therapy ; Mice ; Mice, Inbred C57BL ; Peptides/genetics ; Peptides/immunology ; Positron-Emission Tomography ; Protein Binding ; Protein Engineering/methods ; Receptors, Immunologic/genetics ; Receptors, Immunologic/immunology ; Recombinant Fusion Proteins/genetics ; Recombinant Fusion Proteins/immunology ; Saccharomyces cerevisiae/genetics ; Saccharomyces cerevisiae/metabolism ; Serum Albumin/genetics ; Serum Albumin/immunology ; Skin Neoplasms/diagnostic imaging ; Skin Neoplasms/genetics ; Skin Neoplasms/mortality ; Skin Neoplasms/therapy ; Survival Analysis ; Tumor Burden/drug effects
Chemical Substances	Carrier Proteins ; Interleukin-2 ; Peptides ; Receptors, Immunologic ; Recombinant Fusion Proteins ; Serum Albumin ; collagen-related peptide ; leukocyte-associated immunoglobulin-like receptor 1 ; Collagen (9007-34-5)
Language	English
Publishing date	2022-01-10
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-021-27390-6
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