Manganese complexes and manganese-based metal-organic frameworks as contrast agents in MRI and chemotherapeutics agents: Applications and prospects

doi:10.1016/j.colsurfb.2022.112432

Colloids and Surfaces B: Biointerfaces

Volume 213, May 2022, 112432

https://doi.org/10.1016/j.colsurfb.2022.112432 Get rights and content

Highlights

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Mn-MOFs are divided into three categories based on their multidisciplinary applications.
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Mn-based materials employed as a potential MRI agent due to their strong targeting ability.
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Representative examples of these characteristics and mechanisms have been illustrated.
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These applications of CDT, SDT and PDT therapy for Mn-MOFs have discussed.

Abstract

Manganese-based Metal-organic Frameworks (Mn-MOFs) represents a unique sub-class of MOFs with low toxicity, oxidative ability, and biocompatibility, which plays vital role in the application of this class of MOFs in medical field. Mn-MOFs show great potential in biomedical applications, and has been extensively studied as compared to other MOFs in transition metal series. They are important in medical applications because Mn(II) possess large electron spin number and longer electron relaxation time. They display fast water exchange rate and could be employed as a potential MRI contrast agent because of their strong targeting ability. Manganese complexes with different ligands also display prospective applications in area such as carrier for drug targeting in anti-tumor and antimicrobial therapy. In the review presented herewith, the application of Mn-based complexes and Mn-MOFs have been emphasized in the area such as imaging viz. MRI, multimodal imaging, antitumor activities such as chemodynamic therapy, photodynamic therapy, sonodynamic therapy and antimicrobial applications. Also, how rational designing and syntheses of targeted Mn-based complexes and Mn-MOFs can engender desired applications.

Graphical Abstract

Introduction

Metal-Organic Frameworks (MOFs) are porous three-dimensional (3D) crystalline materials with periodic network structure formed by self-assembly of metal ions or metal clusters and organic ligands through coordinate bonds formation between both units. This kind of inorganic/organic hybrid material exhibited excellent performance, which could be credited to their high specific surface area, adjustable size and porosity with ease of surface modification. Therefore, this class of materials are widely used in catalysis, gas storage, multiphase catalysis, drug delivery, chemical sensing and other fields [1]. Likewise, coordination complexes are formed by the combination of central metal atoms (or ions, collectively referred to as central metal atoms) and molecules or ions surrounding them (called ligands / ligands) completely or partially through coordination bonds. Compared to other transition metal [2], manganese is an essential human dietary element, important in macronutrient metabolism, bone formation, and free radical defense systems. It is a critical component in dozens of proteins and enzymes [3]. It is found mostly in the bones and also is an important constituent of liver, kidneys, and brain. In human brain, the manganese bound to manganese metalloproteins, most notably glutamine synthetase in astrocytes [3].

Amongst varied class of MOFs, the manganese based organic framework (Mn-MOFs) tend to form common secondary structural units and topographic structure, so they could be better designed to realize the targeted structure, function and eventual application. Compared with other transition metal-based MOFs, Mn-MOFs have the following advantages: (1) Mn-MOFs are biocompatible, easily excreted through the kidneys, and have low toxicity. Moreover, Mn is one of the essential trace elements in the normal organism and is involved in the growth and development of many tissues as well as the metabolism of substances in the body [4], [5], [6]; (2) Owing to the presence of more unpaired electrons in the five d orbitals of Mn ions (especially Mn²⁺ and Mn³⁺), they have stronger paramagnetic character, thus giving Mn-MOFs a strong relaxation enhancement effect and hence they find potential as contrast agents (CAs) [7a]; (3) Mn-MOFs have strong redox activity, and utilizes pH and oxidation potential as imaging triggers to achieve a special response to the tumor microenvironment while improving and assisting tumor treatment [7a]. Manganese plays an important role as an activator and essential cofactor of enzymes in biology, especially for bone development, cell structure, energy metabolism, mitochondrial redox and apoptosis [7b]. Many studies have reported that Mn can bind DNA, RNA and ribosomes to cause protein transcription and translation disorders [7c]. In recent years, Mn, as the central ion in varied complexes, has attracted extensive attention as it effectively regulate cell metabolism. Till now, plethora of MOFs have been reported which exhibited different structural characteristics and displayed manifold applications in materials science and biological chemistry [8]. With these aspects in mind, in the presented perspective, an overview related to the investigation on Mn-MOFs and Mn-complexes have been presented and their application in imaging, antitumor and antibacterial have been accounted. Importantly, the perspective provides an overview about the rational designing, syntheses and targeted applications of Mn-MOFs and Mn-complexes with apt examples (Scheme 1).

Section snippets

Imaging

Magnetic resonance imaging (MRI), a non-invasive imaging technique with high spatial resolution is an effective whole-body imaging technique [39]. It can be used to reveal the detailed information related to tumor, including the location and size of the tumor, before undergoing in vivo photo-chemotherapy to minimize the side effects of treatment, and hence is widely used in the early diagnosis and monitoring of tumors [19]. This technique is based on the principles of nuclear magnetic resonance

Conclusion

In the presented perspective, we have reviewed the applications of Mn-MOFs and manganese complexes for imaging, anti-tumor and antibacterial applications, and found that the application of Mn-MOFs in imaging largely depend on the nature of framework and chemical properties of Mn-MOFs which of-course is decided by the ligand structures. The ligand’s structure, rigidity and donor-acceptor characteristics affect the thermodynamics, kinetics and redox stability of the resulting Mn-MOFs. The

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This research was partially funded by Guangdong Province Universities and Colleges Pearl River Scholar Fund (No. 4SG21006G), Guangdong Basic and Applied Basic Research Foundation (2019A1515110260), Guangdong Basic and Applied Basic Research Foundation (2021A1515011616), Scientific research project of Traditional Chinese Medicine Bureau of Guangdong Province (20211227), Featured Innovation Project of Guangdong Province (2019KTSCX052 and 2019KTSCX053) and Special Funds for Scientific

References (121)

M. He et al.
ACS Appl. Mater. Interfaces
(2019)
J.J. Xue et al.
Nanomedicine
(2018)
A. Singh et al.
Catal. Sci. Technol.
(2021)
Y. Pan et al.
CrystEngComm
(2019)
J.-Q. Liu et al.
Coord. Chem. Rev.
(2020)
K.G. Liu et al.
J. Am. Chem. Soc.
(2020)
G. Li et al.
Inorg. Chem. Commun.
(2021)
K.G. Liu et al.
Inorg. Chem.
(2020)
J. Wankar et al.
Adv. Funct. Mater.
(2020)
K.G. Liu et al.
J. Mater. Chem. A
(2020)
M.L. Hu et al.
Coord. Chem. Rev.
(2019)
S. Xian et al.
Small
(2021)
H. He et al.
Coord. Chem. Rev.
(2018)
R.M. Colodrero et al.
Chem
(2009)
M.L. Hu et al.
Inorg. Chem. Front.
(2020)
S. Rojas et al.
J. Mater. Chem. B
(2017)
L. Esrafili et al.
J. Hazard. Mater.
(2021)
S.J. Wang et al.
Mater. Lett.
(2021)
D.J. Levine et al.
J. Am. Chem. Soc.
(2016)
Z. Zheng et al.
Chem. Eng. J.
(2020)
S.S. Wan et al.
ACS Nano
(2019)
P. Geng et al.
Adv. Healthc. Mater.
(2021)
N. Rastogi et al.
J. Inorg. Biochem.
(2017)
B. Phukan et al.
Inorg. Chem.
(2018)
M. Paul et al.
Chemistry
(2016)
Y. Wu et al.
Biomater. Sci.
(2020)
M.K. Islam et al.
Bioconjug. Chem.
(2018)
Z.Y. Ding et al.
Nano Lett.
(2019)
G.Z. Zhao et al.
ACS Omega
(2018)
J. Crowston et al.
Dalton Trans.
(2019)

M. Wu et al.

Nanotechnology

(2015)

X.T. Pan et al.

Angew. Chem. Int. Ed.

(2020)

M.K. Bhattacharyya et al.

J. Inorg. Biochem.

(2019)

C. Icsel et al.

Eur. J. Med. Chem.

(2020)

S. Cao et al.

Chem. Commun.

(2019)

V. P et al.

J. Photochem. Photobiol. B

(2018)

D. Musib et al.

Appl. Organomet. Chem.

(2020)

W.H. Mahmoud et al.

J. Mol. Struct.

(2015)

Y.P. Hao et al.

Polyhedron

(2018)

C. Peter

Chem. Soc. Rev.

(2006)

S.L. O’Neal et al.

Curr. Environ. Health Rep.

(2015)

Mário J.F. Calvete et al.

Coord. Chem. Rev.

(2017)

C. Peter et al.

Contrast Media Mol. Imaging

(2009)

H.X. Zhao et al.

ACS Appl. Mater. Interfaces

(2021)

P. Zhao et al.

Dyes Pigment.

(2016)

B.J.M. Leite Ferreira et al.

J. Inorg. Biochem.

(2016)

H. Moon et al.

Chem. Sci.

(2018)

K.T. Butterworth et al.

Nanoscale

(2012)

M. Nasrabadi et al.

New J. Chem.

(2019)

M. Chen et al.

Small

(2020)

S. Xian et al.

Small

(2021)

Y. Zhao et al.

Rare Met.

(2021)

J.H. Qin et al.

Dalton Trans.

(2020)

J.H. Qin et al.

Inorg. Chem.

(2019)

H. Furukawa et al.

Science

(2013)

Q.L. Zhu et al.

Chem. Soc. Rev.

(2014)

L.E. Kreno et al.

Chem. Rev.

(2012)

A. Dutta et al.

Coord. Chem. Rev.

(2021)

W.C. Liu et al.

Chem. Eng. J.

(2021)

M.L. Hu et al.

J. Hazard. Mater.

(2021)

K.M. Erikson et al.

Met. Ions Life Sci.

(2019)

W.B. Yao et al.

Org. Chem. Front.

(2021)

S.Y. Liu et al.

Org. Chem. Front.

(2018)

A.B. Xia et al.

New J. Chem.

(2015)

S.Y. Liu et al.

Dyes Pigment.

(2019)

John Emsley, Oxford University Press, Oxford, UK, 2001, pp....

J.L. Aschner et al.

Mol. Asp. Med.

(2005)

K.M. Erikson et al.

Environ. Toxicol. Pharmacol.

(2004)

C.L. Keen et al.

Neurotoxicology

(1999)

García-Hevia Lorena et al.

Chem. Eur. J.

(2018)

M.R. Smith et al.

Biochem. Biophys. Res. Commun.

(2017)

T.E. Cunter et al.

Toxicol. Appl. Pharmacol.

(2010)

T.E. Hutchinson et al.

Inorg. Chim. Acta

(2019)

F.K. Kalman et al.

J. Med. Chem.

(2020)

K. Sarkar et al.

Chem. Eur.

(2016)

D. Zhang et al.

Chem. Sci.

(2018)

G. Paul et al.

Chem. Commun.

(2014)

J.H. Wang et al.

Angew. Chem.

(2018)

Q.Y. Chen et al.

Sci. China Chem.

(2010)

Z.H. Meng et al.

J. Colloid Interface Sci.

(2021)

P. Promdet et al.

Dalton Trans.

(2018)

F. Ye et al.

Biomaterials

(2014)

M.Q. Yang et al.

Dyes Pigment.

(2019)

K. Sarkar et al.

ACS Appl. Mater. Interfaces

(2018)

D.D. Wang et al.

Chem. Mater.

(2017)

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Manganese complexes and manganese-based metal-organic frameworks as contrast agents in MRI and chemotherapeutics agents: Applications and prospects

Highlights

Abstract

Graphical Abstract

Introduction

Section snippets

Imaging

Conclusion

Declaration of Competing Interest

Acknowledgments

ACS Appl. Mater. Interfaces

Nanomedicine

Catal. Sci. Technol.

CrystEngComm

Coord. Chem. Rev.

J. Am. Chem. Soc.

Inorg. Chem. Commun.

Inorg. Chem.

Adv. Funct. Mater.

J. Mater. Chem. A

Coord. Chem. Rev.

Small

Coord. Chem. Rev.

Chem

Inorg. Chem. Front.

J. Mater. Chem. B

J. Hazard. Mater.

Mater. Lett.

J. Am. Chem. Soc.

Chem. Eng. J.

ACS Nano

Adv. Healthc. Mater.

J. Inorg. Biochem.

Inorg. Chem.

Chemistry

Biomater. Sci.

Bioconjug. Chem.

Nano Lett.

ACS Omega

Dalton Trans.

Nanotechnology

Angew. Chem. Int. Ed.

J. Inorg. Biochem.

Eur. J. Med. Chem.

Chem. Commun.

J. Photochem. Photobiol. B

Appl. Organomet. Chem.

J. Mol. Struct.

Polyhedron

Chem. Soc. Rev.

Curr. Environ. Health Rep.

Coord. Chem. Rev.

Contrast Media Mol. Imaging

ACS Appl. Mater. Interfaces

Dyes Pigment.

J. Inorg. Biochem.

Chem. Sci.

Nanoscale

New J. Chem.

Small

Small

Rare Met.

Dalton Trans.

Inorg. Chem.

Science

Chem. Soc. Rev.

Chem. Rev.

Coord. Chem. Rev.

Chem. Eng. J.

J. Hazard. Mater.

Met. Ions Life Sci.

Org. Chem. Front.

Org. Chem. Front.

New J. Chem.

Dyes Pigment.

Mol. Asp. Med.

Environ. Toxicol. Pharmacol.

Neurotoxicology

Chem. Eur. J.

Biochem. Biophys. Res. Commun.