Biotechnol Lett (2015) 37:491–498 DOI 10.1007/s10529-014-1728-6

REVIEW

Magnetotactic bacteria for cancer therapy Abhilasha S. Mathuriya

Received: 5 August 2014 / Accepted: 6 November 2014 / Published online: 12 November 2014 Ó Springer Science+Business Media Dordrecht 2014

Abstract Cancer is characterized by anomalous cell growth. Conventional therapies face many challenges and hence alternative treatment methods are in great demand. In addition, nature offers the best inspiration and recently many therapies of natural origin have proved multi-targeted, multi-staged, and a multicomponent mode of action against cancer. Magnetotactic bacteria and magnetosomes-based treatment methods are among them. Present paper reviews various routes by which magnetotactic bacteria and magnetosomes contribute to cancer therapy. Keywords Bacteria and cancer  Drug delivery  Hyperthermia  Magnetotactic bacteria  Magnetosomes

Introduction Cancer is characterized by anomalous and invasive cell growth. A cancer becomes incurable when it spreads to other parts of the body in a process called metastasis. Many conventional anti-cancer therapies, viz. surgical, radio- and chemotherapy, are available to cure or stop cancer growth (Patyar et al. 2010). One

A. S. Mathuriya (&) Department of Biotechnology, Anand Engineering College, NH-2, Keetham, Agra 282007, India e-mail: [email protected]

of the major lacunas in these therapies is the generation of resistance that creates a need for alternative therapies. Many other alternate therapies, viz. gene therapy, dichloroacetate therapy, complementary therapy, insulin-potentiating therapy and bacterial treatment (Jain 2001), are also available. All these therapies have their inherent potentials and sideeffects. There is a need for more effective cancer treatments with fewer side effects. Recently nanotechnology has opened many doors in cancer therapy. Magnetotactic bacteria (MTB) and their magnetosomes are among those solutions which offer great promise in cancer therapy in various ways. MTB are ubiquitous, aquatic and motile bacteria that mineralize magnetosome—a forte organelle with nano-sized magnetic magnetite (Fe3O4) or greigite (Fe3S4) crystals in various arrangements (Arakaki et al. 2008). These crystals are enclosed by a membrane containing phospholipids, phosphatidyl ethanolmine, phosphatidyl glycerol, some amino groups and specific proteins. This membrane controls the crystal size and morphology and generates a matrix for the function and stability of magnetosomes and therefore, magnetosomes can act as biogenic material with high bio- and nano-technological potential (Arakaki et al. 2008). MTB (the entire living cell) and magnetosomes both offer applications in various areas of cancer treatment (Yoshino et al. 2010) in different ways (Fig. 1). Although commercially-available iron oxide particles are produced via chemical synthesis, yet they

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Fig. 1 Application of magnetotactic bacteria and magnetosomes in cancer therapy

cannot compete with magnetosomes in terms of their intrinsic magnetic features, genetically-controlled uniform nano-morphology, narrow size distributions, having a biomembrane envelope (Arakaki et al. 2008; Yoshino et al. 2010; Hofer 2013; Alphandery 2014). This review is an attempt to summarize the applicability of the MTB and magnetosomes in the various areas of cancer treatment.

Drug delivery systems Chemotherapy is an effective therapy against active cancer cells using anti-cancer drugs, singly or in combination. However, it leads to damage healthy cells, such as blood and hair cells. As anti-cancer drug administration inhibits or stops cell growth, the concentrations of the drug should be below a toxic level and above a level of minimal therapeutic effect.

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Unfortunately, the human body does not have the ability to segregate these spatio-targeted profiles and therefore drugs distribute throughout the body and can affect healthy organs which do not require drug treatment. In addition, the body’s defence mechanism generally excretes foreign substances (Kingsley et al. 2006). To meet these challenges, many research groups have investigated drug delivery systems that use more biocompatible and biodegradable materials to control the drug release from microstructures to reduce the side-effects (Sahoo and Labhasetwar 2003; Sinha et al. 2006; Suri et al. 2007). The concept of such an efficient system is to locate drugs at the targeted site, and at the required concentration for the right period of time (Kingsley et al. 2006). Recently, MTB and magnetosomes have proved their candidature (Schu¨ler and Frankel 1999; Hopkin 2004; Martel 2006, 2014; Munoz-Jimenez et al. 2010) as smart drug carriers due to their unique

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characteristics such as para-magnetism, uniform nano size, narrow size distribution and being membrane bound (Gorby et al. 1988; Nakamura et al. 1991; Bazylinski et al. 1994; Hoell et al. 2004; Grunberg et al. 2004). Magnetosomes contain amino groups and glycerol on their membrane surface, which allows them to be coupled to another ligand. Therefore, magnetosomes can act as efficient drug carriers with a higher drug loading ratio than some artificial magnetic particles. Magnetoliposomes, containing cis-diammine-dichloro-platinum(II) (cisplatin: platinumcontaining anti-cancer drug) coupled with magnetosomes, have been evaluated for drug targeting and controlled release at tumor sites (Matsunaga et al. 1997). The capture volume of the magnetoliposomes was 1.7 times higher than that of artificial magnetic particles. In addition, magnetoliposomes released their content over 2 h on application of a rotating magnetic field (Matsunaga et al. 1997). In another study (Deng et al. 2013), cytosine arabinoside (Ara-C) was combined with magnetosomes via cross-linking with genipin. The results exhibited about 90 % encapsulation efficiency and 47 % drug loading efficiency, for 72 h. The Ara-C system showed a long-term stability, and 80 % of the drugs could be released over 3 months without an initial burst. Accurate drug delivery to target organs is a critical need for a successful, cell-based therapy by stem cells or immune cells. Contrast-agent labelling before implantation can be a powerful tool for observing cellular actions by MRI. Schwarz et al. (2009) investigated magnetosomes uptake into dendritic cells and hematopoietic Flt3? stem cells from the bone marrow of mouse and observed that uptake of magnetosomes into the cells increased magnetic activity; cells loaded with magnetosomes were promptly detected by MRI. Radiotherapy is the application of radiations, viz. gamma rays, X-rays, electron beam to weaken or stop cancer cell from further growth and multiplication (Kumar et al. 2009). Magnetosomes could also be coupled to radioactive isotopes, e.g. using chelates, radioactive-labelled molecules, such as nucleic acids and proteins (Sun et al. 2011), and would offer a better internal radiation of solid tumors because of their accurate targeted delivery (Sun et al. 2011). Further, (Sun 2007; Sun et al. 2008) doxorubicin was loaded onto bacterial magnetosomes (DBMs) in EMT-6 and HL60 cell-lines to study in vitro and in vivo anti-

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neoplastic effects on hepatic cancer. DBMs showed a slower doxorubicin release into serum and maintained 80 % stability up to 48 h of incubation. Liu et al. (2013), loaded methotrexate and genipin onto magnetosomes with about 50 % drug loading, up to 98 % encapsulation efficiency and stable drug release.

G protein-coupled receptors (GPCRs) expression G protein-coupled receptors (GPCRs) are the largest family of membrane proteins in the human genome. They have applications in drug discovery, cancer treatment, endocrine, neural and other disorders (Katritch and Abagyan 2011). GPCRs contain many hydrophobic domains which cause complexities in the purification of GPCRs from cells and in the loss of native conformation. The GPCR with natural conformation was manufactured by expression of the GPCR gene in MTB (Matsunaga et al. 2004). The GPCR gene was expressed as a chimeric gene coding for the GPCR and anchor protein which was selected from magnetite particle membrane proteins of their fragments. Yoshino et al. (2002) used D1R as a model GPCRs and fused it to magnetosomes-membrane-specific-protein Mms16. Further, GPCRs were also assembled into the lipid membrane of magnetosomes of M. magneticum AMB-1 (Yoshino et al. 2004).

Single nucleotide polymorphisms (SNPs) SNPs are human genetic polymorphisms that help in the identification of genes associated with diseases such as cancer, and diabetes (Tomita-Mitchell et al. 1998). To produce accurate data, SNP analysis requires large sample, therefore high-throughput and accurate multiple-assay system is required for SNP analysis (Tomita-Mitchell et al. 1998). Maruyama et al. (2004) developed a protocol based on DNA thermal dissociation curve analysis for an automated system with magnetosomes by developing a new method for avoiding light scattering caused by nanometer-size particles when using commercially-available fluorescent dyes such as FITC, Cy3, and Cy5 for labeling chromophores. SNPs of aldehyde dehydrogenase-2 (Maruyama et al. 2004), epidermal growth factor receptor (Maruyama 2007) and transforming growth factor b-1 (Ota et al. 2003; Matsunaga et al.

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2007) genes have been detected. In another study, a semi-automated SNPs detection system, based on thermal-dissociation-curve-analysis and allele-specific oligonucleotide hybridization using magnetosomes was developed by Matsunaga et al. (2007).

Magnetic fluid hyperthermia Hyperthermia treatment of tumors is one of the most promising biomedical applications for the treatment of some causes. In this treatment, heat-sensitive tumor cells are destroyed by high temperatures (Hergt et al. 2006). Hyperthermia is applied in conjugation with other methodologies such as radiotherapy and chemotherapy. Hyperthermia facilitates increased oxygenation and perfusion of neoplastic hypoxic cells which leads to increased absorption of chemotherapeutic drugs (Dutz and Hergt 2013). Microwave hyperthermia cancer treatment in conjunction with radiation, has been approved by Food and Drug Administration (Luk et al. 1986). Non selective heating by chemical metal nano particles (MNP), cause damage to surrounding healthy tissue and pose severe side effects. Therefore, there is a need for significantly improved and more selective hyperthermia agents and procedures for uniformly controlled induction heating, and prevention of the necrosis of normal tissue (Alphandery et al. 2013). An important characteristic of magnetosomes is their ability to generate heat on application of an oscillating magnetic field. This feature conceives the idea that these magnetosomes might be applicable in the destruction or inactivation of tumor cells through hyperthermia or thermoablation (Alphandery et al. 2011a). Alphandery et al. (2011a) reported the heating efficiency and magnetic properties of cobalt-doped magnetosomes for applications in hyperthermiabased, magnetic field cancer therapy. The hysteresis losses, magnetic properties and heating efficiency of the magnetosome chains were enhanced after cobalt doping. Further hyperthermia treatment of mouse tumor by magnetosomes by applying an alternative magnetic field was also described (Alphandery et al. 2011b). In addition, Alphandery et al. (2011c) studied the heat production capabilities of MTB cells, extracted chains of magnetosomes, and extracted individual magnetosomes without membranes, when exposed to an oscillating magnetic field. The specific

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heat absorption rates of all of those samples were higher than that of super-paramagnetic nanoparticles. Further, MDA-MB-231 breast cancer cells incubated with magnetosomes with a 183 kHz frequency alternative magnetic field with field strengths of 20, 40, or 60 mT, were almost completely destroyed (Alphandery et al. 2011d). Some research groups (Liu et al. 2012; Alphandery et al. 2012) are applying magnetosomes in magnetic fluid hyperthermia in different ways.

Magnetic resonance imaging (MRI) MRI is a technique that demonstrates non-invasive molecular imaging of cells and cellular activities. It can monitor cellular processes such as cancer growth and metastasis (Goldhawk et al. 2012). The MRI approach is favoured as it: (a) provides non-invasive details, (b) allows simultaneous tracking and actuation of the nanoparticles, (c) provides very specific localization of the magnetic particles, and (d) is readily available at most hospitals. In MRI, cell tracking methods involve exogenous labels, like super-paramagnetic iron-oxide nanoparticles, that however, are degraded by the cellular activities like mitosis and therefore lack an inherent biological function (Goldhawk et al. 2012). Magnetosomes can also be used as MR contrast agents for cell tracking and imaging as they can differentiate between healthy and pathological tissues. Herborn et al. (2003) characterized magnetosomes as super-paramagnetic contrast agents for MRI and their longitudinal and transverse relaxivities were calculated to be 7.688 and 147.67 mmol-1 s-1. Lisy et al. (2007) assessed the use of fluorochrome-coupled magnetosomes (FCM) as bimodal contrast agent for both MRI and near-infrared fluorescence optical imaging of cultured macrophages. FCM showed higher fluorescence intensities above 670 nm. Further, macrophages could also be labelled with FCM and were imaged using both a 1.5 T MR scanner and nearinfrared fluorescence imaging. Felfoul et al. (2007) studied application of MTB as bio-carriers for drug delivery, and observed that the magnetosomes in MTB could track bacterial displacement in vivo using MRI. In another study, the in vitro and in vivo ability of M. magneticum AMB-1 as MRI contrast was determined (Benoit et al. 2009): AMB-1 could produce positive

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MRI contrast and colonize mouse tumor xenografts. Felfoul et al. (2010) observed that magnetosomes were predominant sources of contrast in MRI. Goldhawk et al. (2012) reviewed the magnetosomes as reporters of gene expression in MRI and found their suitability and superiority. Vereda et al. (2009) also reported the application of magnetosomes as MRI contrast agent. In their patent application, Gambhir et al. (2010) disclosed the use of M. magneticum AMB-1 as an MRI contrast agent and a method of tumor detection using MTB enhancement for the positive contrast of MRI. Afkhami et al. (2011) developed a method for MTB encapsulation by magnetic resonance navigation in a controlled release pattern and its carriage towards the capillary network area where they could released and guided towards the tumor.

Robotics or actuators The microrobot construction within the 1–2 lm range using only artificial components is difficult due to several technological obstructions. Therefore, there is a need to find a biological entity having an embedded power and propulsion system. Technically, MTB can act like micro-robots as they possess an efficient molecular motor, sensory and actuation capabilities as well as an embedded remote control interface (Martel 2012). Motile MTBs having flagella are responsible for the actuation and propulsion. They can therefore propel and steer micro-devices, and nanorobots under computer control. For an example, MC-1 MTBs propelled themselves with flagella generating a thrust exceeding 4 pN (Lu and Martel 2006). If this ability could be coupled with appropriate computer-controlled magnetic fields of a few Gausses, it can perform tasks on nanometric scale (Lu and Martel 2006). Martel et al. (2009) described several medical robots that performed efficiently through suitable software/hardware subsystems in the microvasculature modules. This methodology allowed higher targeting efficacy and operations in locations as tumoral lesions which were accessible only through complex microvasculature networks. Mokrani et al. (2010) studied the ability of MTBs to penetrate 3D multi-cellular tumor spheroids. This model showed that MTB could be navigated in tumor environments and act as a microrobot for drug delivery under computer magnetic field.

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Magnetic resonance targeting (MRT) is among latest technologies in medical robotics that facilitates enhanced target interventions in the human body. It uses MRI to receive tracking data and to determine the position of entities and guide them towards a specific location in the body through the vascular network. Microrobotic navigable entities for MRT were studied by Martel (2010) to target colorectal tumors by controllable MTBs having propelling thrust force by two flagella exceeding 4 pN, i.e. a tenfold increase over typical flagellated bacteria. Felfoul et al. (2011) reported computer-controlled MTB navigation towards solid tumors with 300 lm s-1 swimming velocities, without an external power source. Khalil et al. (2013a) studied closed-loop control strategy for MTBs-based microrobots. Khalil et al. (2013b) also demonstrated that this control system positioned an MTB at an average velocity of 28 lm s-1, within an average region-of-convergence of 40 lm.

Perspectives Although MTBs and magnetosomes can help in cancer treatment in different ways, they are still rarely employed in vivo as drug carriers. This is due to their uncertain biocompatibility and pharmacokinetics. Magnetosomes can be considered biocompatible due to: (i) their biological origin (Xiang et al. 2007), (ii) negligible chemical toxicity (Hafeli and Pauer 1999; Wagner et al. 2006), and (iii) insolubility of Fe3O4. Magnetosomes are enclosed by a lipid bilayer and specific soluble and trans-membrane proteins helps magnetosomes to attain biocompatibility. On the other hand, toxic properties of magnetosomes might be due to: (i) their nano-scale size, which leads to deposition and aggregation of nanoparticles in the body (Sun et al. 2010), (ii) impurities (particularly proteins, nucleic acids, and polysaccharides) associated with magnetosomes during extraction from cells, and their immunotoxicity, and (iii) membrane-containing proteins (Jevprasesphant et al. 2003; Grunberg et al. 2004). Many scientists have studied in vivo and in vitro biocompatibility of magnetosomes in target cells (Xiang et al. 2007; Sun 2009; Liu et al. 2012; Taherkhani et al. 2014). Xiang et al. (2007) evaluated in vitro cytotoxicity of magnetosomes for mouse fibroblasts and observed that magnetosomes were not toxic. A target distribution

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of magnetosomes in the sublingual vena of SpragueDawley rats was observed by Sun (2009) and the distributions of magnetosomes in dejecta (liquid or solid waste matter, shed or discharged from the body), serum, urine and in other main organs were examined. After injection, the presence of magnetosomes was observed only in the liver and no evidence of the magnetosome existence was observed in the dejecta and urine during 72 h after intravenous administration. In addition, histological examination of major organs of rats showed no remarkable pathological changes except thicker interlobular septa in lungs and increased number of vacuoles in livers (Sun 2009). In another study, hemolysis assay, MTT test, and micronucleus test were conducted by Yan (2012). Magnetosomes up to 4 mg ml-1 showed no cytotoxic, genotoxic, and hemolytic effects, claiming good biocompatibility. Cytotoxicity studies on human breast cancer cells MCF-7 were conducted by Liu et al. (2012) and, although cell viability was decreased by the heat derived from magnetosomes, lower toxicities under an alternative magnetic field was observed. Taherkhani et al. (2014) observed that liposomal attachments to MTB formulation improved the biocompatibility of MTB, whereas attachment does not interfere with liposomal uptake. The lack of international guidelines to evaluate the toxicity of nanomaterials (Malloy 2011) is responsible for the lag in commercialization of MNPs-based products and processes. Additionally, the production of MTBs must comply with the industrial and healthcare requirements. If these lacunas are overcome, MTBs and magnetosomes will certainly play an important role in cancer therapy in the near future due to their superior analytical performance, novel characteristic features, and a plethora of applications. Acknowledgment Author acknowledges Mr. Anshul Kumar for editing this manuscript.

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Magnetotactic bacteria for cancer therapy.

Cancer is characterized by anomalous cell growth. Conventional therapies face many challenges and hence alternative treatment methods are in great dem...
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